ArticlePDF Available

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

Authors:

Abstract and Figures

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.
Content may be subject to copyright.
1
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
IMPACT OF OCEAN WARMING AND OCEAN
ACIDIFICATION ON MARINE INVERTEBRATE LIFE
HISTORY STAGES: VULNERABILITIES AND POTENTIAL
FOR PERSISTENCE IN A CHANGING OCEAN
MARIA BYRNE
Schools of Medical and Biological Sciences, University of Sydney, Australia
E-mail: mbyrne@anatomy.usyd.edu.au
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.
Introduction
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,
MARIA BYRNE
2
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
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
3
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
Juvenile
Spawning
Fertilized embryo
Advanced brachiolaria
Development
Bipinnaria Brachiolaria
Gastrula
Cleavage
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.)
MARIA BYRNE
4
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
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
5
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)
Reference
Range for
fertilization of
75% or more
Temperature
increase above
local ambient
for fertilization
<70–75%
pH range for
fertilization of
75% or more
pH at which
fertilization
is reduced to
<70–75%
Cnidaria
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
Nemertea
Parborlasia corrugatus 0–1 ND 7.0–8.0
528–5806 ND Ericson et al. 2010
Polychaeta
Galeolaria caespitosa 21 5 ND ND Kupriyanova &
Havenhand 2005
Nereis virens 10–18 15 ND ND Lewis et al. 2002
Mollusca
Gastropoda
Haliotis coccoradiata 20–24 ND 7.6–8.2
327–1795
ND Byrne et al. 2010b
Bivalvia
Crassostrea gigas 18–30 ND 7.4–8.2
≤2000
ND Kurihara et al.
2007, Kurihara
2008, Havenhand
& Schlegal 2009
18–30 ND 7.9–8.2
375–750
7.8
1000
Parker et al. 2010
Mytilus galloprovincialis 13 ND 7.4–8.0
≤2000
ND Kurihara 2008
Saccostrea glomerata 26 >4 8.0–8.2
375–600
7.9
750
Parker et al. 2010
Spisula solidissima 8–20 >10 ND ND Clotteau & Dubé
1993
Echinodermata
Asteroidea
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)
MARIA BYRNE
6
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)
Reference
Range for
fertilization of
75% or more
Temperature
increase above
local ambient
for fertilization
<70–75%
pH range for
fertilization of
75% or more
pH at which
fertilization
is reduced to
<70–75%
Patiriella regularis 20–26 ND 7.6–8.2
330–1828
ND Byrne et al. 2010b
Meridiastra calcar 18–23 ND 7.6–8.2
330–1828
ND Nguyen, H. pers.
comm.
Echinoidea
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
324–1695
ND Byrne et al. 2010b
Dendraster excentricus 7–26 13 ND ND Bingham et al.
1997
Diadema savignyi 28–36 >8 ND ND Rupp 1973
Echinometra lucunter 15–36 9 ND ND Sewell & Young
1999
Echinometra mathaei 28–36 8 7.7–8.1
360–1360
7.3
2360
Rupp 1973,
Kurihara &
Shirayama 2004
Heliocidaris erythrogramma 17–26 ND 7.6–8.2
327–1729
ND Byrne et al. 2009,
2010a,b, 2011a,b
Heliocidaris tuberculata 17–24 ND 7.6–8.2
327–1729
ND O’Connor &
Mulley 1977,
Byrne et al.
2010b
Hemicentrotus pulcherrimus 0–30 15 7.4–8.0
360–2000
6.8–7.0
2000–10,000
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
527–1121
7.0–7.3a
2886–5806
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
332–1765
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.
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
7
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
100
80
60
40
% Fertilization
20
0
100
80
60
40
20
0
100
80
60
40
20
0
pH 8.2
327–335 814–851 1051–1104 1729–1828 327–335 1051–1104 1729–1828
PCO2
7.9 7.8 7.6 8.2 7.8 7.6
18
20
22
24
26
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.)
MARIA BYRNE
8
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
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
9
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
MARIA BYRNE
10
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)
Reference
Optimum range for
development
(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
development
Low pH/ pCO2 effects on
embryos, larvae or juvenilesEmbryos Larvae Embryos Larvae
Porifera
Rhopaleoeides odorabile 22–28 22–28 10 10 ND ND Whalan et al. 2008
Cnidaria
Acropora digitata 27 ND ND NS 7.3–8.0
400–3585
7.3/3500
Smaller polyps
Suwa et al. 2010
7.3–7.6
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
400–3585
7.3–7.6/900–3585
Smaller polyps
Kurihara 2008, Suwa et al.
2010
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
Nemertea
Parborlasia corrugatus 0–1 ND ND ND 7.3–8.0
528–2886
7.0/5806 Ericson et al. 2010
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
11
Mollusca
Gastropoda
Haliotis coccoradiata 20–22 20 4 2–4 8.0–8.2
327–420
7.6–7.8/1080–1729
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
Bivalvia
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
291–823
ND Miller et al. 2009
Crassostrea gigas 18–30 18–30 ND ND 7.8–8.2
375–1000
7.4/2268
Decreased larval calcication
Kurihara et al. 2007, Kurihara
2008
7.8/1000
Abnormal development,
decreased larval calcication
Parker et al. 2010
Crassostrea virginica 20–30 20–30 ND ND 8.0–8.2
284–389
7.76–7.9/572–840 MacInnes & Calabrese 1979,
Wright et al. 1983, Miller
et al. 2009, Talmage & Gobler
2009
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
375–750
7.8–8.0/600–1000
Smaller larvae
Parker et al. 2010, Watson et al.
2009
(continued on next page)
MARIA BYRNE
12
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)
Reference
Optimum range for
development
(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
development
Low pH/ pCO2 effects on
embryos, larvae or juvenilesEmbryos Larvae Embryos Larvae
Cephalopoda
Sepia ofcianalis 17 ND ND ND 7.1–8.0
636–6148
ND Gutowska et al. 2008, 2010a,b
Echinodermata
Ophiuroidea
Ophiothrix fragilis 14 ND ND ND 8.1 7.7–7.9
Smaller larvae
Dupont et al. 2008
Asteroidea
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
372–930
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
330–1762
ND Byrne & Barker 1991,
Foo, 2010
Meridiastra calear 18–21 ND 5 ND Nguyen, H., pers. comm.
Echinoidea
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
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
13
Centrostephanus rodgersii 18–22 18–22 6 ND 7.8–8.2
324–1069
7.6–78/1695–1762 Foo 2010
Dendraster excentricus 7–20 ND 9 ND ND ND Fujisawa 1993, Bingham et al.
1997
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
360–860
7.6/1000
Smaller larvae
Rupp 1973, Kurihara 2008
Evechinus chloroticus 15 ND ND ND 7.7–8.1
438–1320
7.7/1320
Smaller larvae
Clark et al. 2009
Heliocidaris erythrogramma 18–24 18–24 4–6 4–6 7.6–8.2
330–1892
7.6
No effect on early development
Byrne et al. 2009, 2010a,b,
2011a
7.6–7.8/1050–1730
Impaired juvenile calcication
Byrne et al. 2011b
7.7/1000
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
360–860
7.6/1000
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
429–1282
7.7/1282
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
527–2886
7.0/5800
Abnormal blastulae
Stanwell-Smith & Peck 1998,
Ericson et al. 2010
7.6–8.0
521–1380
7.6/1380
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)
MARIA BYRNE
14
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)
Reference
Optimum range for
development
(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
development
Low pH/ pCO2 effects on
embryos, larvae or juvenilesEmbryos Larvae Embryos Larvae
Tripneustes gratilla 16–29 19–31 4 6 7.8–8.25
332–1087
7.6–7.8/1087–1795
Smaller larvae
Clark et al. 2009, Rahman et al.
2009, Sheppard Brennand
et al. 2010
Arthropoda
Acartia erythraea 27 ND ND ND 7.3–8.2
380–2380
6.8–7.0/5000–10,000
Increased mortality
Kurihara et al. 2004
Acartia tsuensis 25 ND ND ND 7.3–8.2
380–2380
ND Kurihara & Ishimatsu 2008
Amphibalanus amphitrite 25–28 ND ND ND 7.4–8.2 7.4
No effect on larvae, smaller
juveniles
McDonald et al. 2009
Calanus nmarchicus 8.8 ND ND ND 6.95–8.23
8000
ND Mayor et al. 2007
Echinogammarus marinus 15 ND ND ND 7.5–8.0
380–1900
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
380–1000
7.6–7.9/1000–1900
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.
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
15
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).
AEB
G
JKLMN
OPQR
HI
CD F
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.)
MARIA BYRNE
16
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
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
17
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
0
20
40
60
80
100
20°C 22°C 24°C
Temperature
% Normal cleaving embryo
pH 8.2
pH 8.0
pH 7.8
pH 7.6
ABC
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.
MARIA BYRNE
18
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
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
19
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.)
MARIA BYRNE
20
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
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
21
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,
MARIA BYRNE
22
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).
Fertilization
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.
Development
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.
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
23
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
MARIA BYRNE
24
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).
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
25
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
MARIA BYRNE
26
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
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
27
(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).
MARIA BYRNE
28
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.
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
29
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.
Acknowledgements
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
the manuscript.
References
Albright, R., Mason, B. & Langdon, C. 2008. Effect of aragonite saturation on settlement and post-settlement
growth of Porites astreoides larvae. Coral Reefs 27, 485–490.
Albright, R., Mason, B., Miller, M. & Langdon, C. 2010. Ocean acidication compromises recruitment success
of the threatened Caribbean coral Acropora palmata. Proceedings of the National Academy of Sciences
of the United States of America 107, 20400–20404.
Allen, J.D. 2008. Size-specic predation on marine invertebrate larvae. Biological Bulletin (Woods Hole) 214,
42–49.
Allen, J.D. & Pechenik, J.A. 2010. Understanding the effects of low salinity on fertilization success and early
development in the sand dollar Echinarachnius parma. Biological Bulletin (Woods Hole) 218, 189–199.
American Society for Testing and Materials (ASTM). 2004. Standard Guide for Conducting Static Acute Toxicity
Tests with Echinoid Embryos E 1563–98. Philadelphia: American Society for Testing and Materials.
Anthony, K.R.N., Kline, D.I., Diaz-Pulido, G., Dove, S. & Hoegh-Guldberg, O. 2008. Ocean acidication
causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of
Sciences of the United States of America 105, 17442–17446.
Arnold, K.E., Findlay, H.S., Spicer, J.I., Daniels, C.L. & Boothroyd, D. 2009. Effects of CO2-related acidication
on aspects of the larval development of the European lobster, Homarus gammarus (L.). Biogeosciences
Discussions 6, 3087–3107.
MARIA BYRNE
30
Baird, A.H., Gilmour J.G.P., Kamiki, T.M., Nonaka, M., Pratchett, M.S., Yamamoto, H.H. & Yamasaki, H. 2006.
Temperature tolerance of symbiotic and non-symbiotic coral larvae. Proceedings of 10th International
Coral Reef Symposium, Okinawa, Japan, 38–42.
Baker, M.C. & Tyler, P.A. 2001. Fertilization success in the commercial gastropod Haliotis tuberculata. Marine
Ecology Progress Series 211, 205–213.
Barnes, D.K.A. & Peck, L.S. 2008. Vulnerability of Antarctic shelf biodiversity to predicted regional warming.
Climate Research 37, 149–163.
Bassim, K.M., Sammarco, P.W. & Snell, T.L. 2002. Effects of temperature on success of (self and non-self) fertil-
ization and embryogenesis in Diploria strigosa (Cnidaria, Scleractinia). Marine Biology 140, 479–488.
Bay, S., Burgess, R. & Nacci, D. 1993. Status and applications of echinoid (Phylum Echinodermata) toxicity
test methods. In Environmental Toxicology and Risk Assessment, ASTM STP 1179, G. Wayne et al. (eds).
Philadelphia: American Society of Testing and Materials, 281–302.
Beniash, E., Ivanina, A., Lieb, N.S., Kurochkin, I. & Sokolova, I.M. 2010. Elevated level of carbon dioxide
affects metabolism and shell formation in oysters Crassostrea virginica. Marine Ecology Progress Series
419, 95–108.
Benitez Villalobos, F., Tyler, P.A. & Young, C.M. 2006. Temperature and pressure tolerances of embryos and
larvae of the Atlantic seastars Asterias rubens and Marthasterias glacialis: potential for deep-sea inva-
sion from the North Atlantic. Marine Ecology Progress Series 314, 109–117.
Bibby, R., Widdicombe, S., Parry, H., Spicer, J. & Pipe, R. 2008. Effects of ocean acidication on the immune
response of the blue mussel Mytilus edulis. Aquatic Biology 2, 67–74.
Bingham, B.L., Bacigalupi, M. & Johnson, L.G. 1997. Temperature adaptations of embryos from intertidal and
subtidal sand dollars (Dendraster excentricus, Eschscholtz). Northwest Science 71, 108–114.
Björk, M., Axelsson, L. & Beer, S. 2004. Why is Ulva intestinalis the only macroalga inhabiting isolated rock-
pools along the Swedish Atlantic coast? Marine Ecology Progress Series 284, 109–116.
Bolton, T.F. & Havenhand, J.N. 1996. Chemical mediation of sperm activity and longevity in the solitary ascid-
ians Ciona intestinalis and Ascidiella aspersa. Biological Bulletin (Woods Hole) 190, 329–335.
Boudry, P., Collet, B., Cornette, F., Hervouet, V., & Bonhomme, F. 2002. High variance in reproductive success
of the pacic oyster (Crossostrea gigas, Thunberg) revealed by microsatellite-based parentage analysis
of multifactorial crosses. Aquaculture 204, 283–296.
Bradshaw, W.E. & Holzapfel, C.M. 2001. Genetic shift in photoperiodic response correlated with global warming.
Proceedings of the National Academy of Sciences of the United States of America 98, 14509–14511.
Brenko, M.H. & Calabrese, A. 1969. The combined effects of salinity and temperature on larvae of the mussel
Mytilus edulis. Marine Biology 4, 224–226.
Bridle, J.R. & Vines T.H. 2006. Limits to evolution at range margins: when and why does adaptation fail?
Trends in Ecology and Evolution 22, 140–147.
Brierley, A.S. & Kingsford, M.J. 2009. Impacts of climate change on marine organisms and ecosystems.
Current Biology 19, 602–614.
Brokaw, C.J. 1990. The sea urchin spermatozoon. BioEssays 12, 449–452.
Buckley, B.A., Owen, M.E. & Hofmann, G.E. 2001. Adjusting the thermostat: the threshold induction tempera-
ture for the heat-shock response of intertidal mussels (genus Mytilus) changes as a function of thermal
history. Journal of Experimental Biology 204, 3571–3579.
Bulling, M.T., Hicks, N., Murray, L., Paterson, D.M., Raffaelli, D., White, P.C.L. & Solan, M. 2010. Marine
biodiversity-ecosystem functions under uncertain environmental futures. Philosophical Transactions of
the Royal Society of London B 365, 2107–2116.
Byers, J.E. & Pringle, J.M. 2006. Going against the ow: retention, range limits ad invasions in advective envi-
ronments. Marine Ecology Progress Series 313, 27–41.
Byrne, M. 2006. Life history evolution in the Asterinidae. 2006. Integrative Comparative Biology 46, 243–254.
Byrne, M. 2010. Impact of climate change stressors on marine invertebrate life histories with a focus on the
Mollusca and Echinodermata. In Climate Alert: Climate Change Monitoring and Strategy, Y. Yu &
A. Henderson-Sellers (eds). Sydney: University of Sydney Press, 142–185.
Byrne, M. & Barker, M.F. 1991. Embryogenesis and larval development of the asteroid Patiriella regularis
viewed by light and scanning electron microscopy. Biological Bulletin (Woods Hole) 180, 332–345.
Byrne, M., Hart, M.W., Cerra, A. & Cisternas, P. 2003. Reproduction and larval of brooding and viviparous
species in the Cryptasterina species complex. Biological Bulletin (Woods Hole) 205, 285–294.
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
31
Byrne, M., Ho, M., Selvakumaraswamy, P., Nguyen, H.D., Dworjanyn, S.A. & Davis, A.R. 2009. Temperature,
but not pH, compromises sea urchin fertilization and early development under near-future climate change
scenarios. Proceedings of the Royal Society Series B 276, 1883–1935.
Byrne, M., Ho, M.A., Wong, E., Soars, N., Selvakumaraswamy, P., Sheppard Brennand, H., Dworjanyn, S.A.
& Davis, A.R. 2011b. Unshelled abalone and corrupted urchins, development of marine calciers in a
changing ocean. Proceedings of the Royal Society Series B DOI: 1098/rspb.2010.2404
Byrne, M., Oakes, D.J., Pollak, J.K. & Laginestra, E. 2008. Toxicity of landll leachate to sea urchin develop-
ment with a focus on ammonia. Cell Biology and Toxicology 24, 503–512.
Byrne, M., Selvakumaraswamy, P., Ho, M.A. & Nguyen, H.D. 2011a. Sea urchin development in a global
change hot spot, potential for southerly migration of thermotolerant propagules. Deep-Sea Research II
58, 712–719.
Byrne, M., Soars, N., Selvakumaraswamy, P., Dworjanyn, S.A. & Davis, A.R. 2010b. Sea urchin fertilization in
a warm, acidied ocean and high pCO2 ocean across a range of sperm densities. Marine Environmental
Research 69, 234–239.
Byrne, M., Soars, N.A., Ho, M.A., Wong, E., McElroy D., Selvakumaraswamy P., Dworjanyn, S.A. & Davis,
A.R. 2010a. Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-
future ocean warming and acidication. Marine Biology 157, 2061–2069.
Byrne, R.H., Kump, L.R. & Cantrell, K.J. 1988. The inuence of temperature and pH on trace metal speciation
in seawater. Marine Chemistry 25, 163–181.
Caldeira, K. & Wickett, M.E. 2003. Anthropogenic carbon and ocean pH. Nature 425, 365 only.
Caldeira, K. & Wicket, M.E. 2005. Ocean model predictions of chemistry changes from carbon dioxide emis-
sions to the atmosphere and ocean. Journal of Geophysical Research 110, C09S04.
Carr, R.S., Biedenbach, J.M. & Nipper, M. 2006. Inuence of potentially confounding factors on sea urchin
porewater toxicity tests. Archives of Environmental Contamination and Toxicology 51, 573–579.
Carroll, S.P., Hendry, A.P., Reznick, D.N. & Fox, C.W. 2007. Evolution on ecological time scales. Functional
Ecology 21, 387–393.
Chen, C.P. & Chen, B.Y. 1992. Effects of high-temperature on larval development and metamorphosis of
Arachnoids placenta (Echinodermata, Echinoidea). Marine Biology 112, 445–449.
Cherr, G.N., Shoffner-McGee, J. & Shenker, J.M. 1990. Methods for assessing fertilization and embryonic/
larval development in toxicity tests using the California mussel (Mytilus californianus). Environmental
Toxicology and Chemistry 9, 1137–1145.
Chia, F.S. & Bickell, L.R. 1983. Echinodermata. In Reproductive Biology of Invertebrates Volume 2, K.G.
Adiyodi & R.G Adiyodi (eds). New York: Wiley, 545–620.
Christensen, A.B., Nguyen, H.D. & Byrne, M. 2011. Thermotolerance and the effects of hypercapnia on the
metabolic rate of the ophiuroid Ophionereis schayeri: inferences for survivorship in a changing ocean.
Journal of Experimental Marine Biology and Ecology DOI: 1001016/j.jembe.2011.04.002
Cigliano, M., Gambi, M.C., Rodolfo-Metalpa, R., Patti, F.P. & Hall-Spencer, J.M. 2010. Effects of ocean acidi-
cation on invertebrate settlement at CO2 volcanic vents. Marine Biology 157, 2489–2502.
Clark, D., Lamare, M. & Barker, M. 2009. Response of sea urchin pluteus larvae (Echinodermata: Echinoidea)
to reduced seawater pH: a comparison among tropical, temperate, and a polar species. Marine Biology
156, 1125–1137.
Clotteau, G. & Dubé, F. 1993. Optimization of fertilization parameters for rearing surf clams (Spisula solidis-
sima). Aquaculture 114, 339–353.
Coma, R., Ribes, M., Serrano, E., Jiménez, E., Salat, J. & Pascual, J. 2009. Global warming-enhanced strati-
cation and mass mortality events in the Mediterranean. Proceedings of the National Academy of Sciences
of the United States of America 16, 6176–6181.
Comeau, S., Gorsky, G., Jeffree, R., Teyssié, J.-L. & Gattuso, J.-P. 2009. Impact of ocean acidication on a key
Arctic pelagic mollusk (Limacina helicina). Biogeosiences 6, 1877–1882.
Compton, T.J., Leathwick, J.R. & Inglis, G.J. 2010. Thermogeography predicts the potential global range of the
invasive European green crab (Carcinus maenas). Diversity and Distributions 16, 243–255.
Cooper, T.F., De’ath, G., Fabricius, K.E & Lough, J.M. 2008. Declining coral calcication in massive Porites in
two nearshore regions of the northern Great Barrier Reef. Global Change Biology 14, 529–538.
Cotter, A.J.R., Phillips, D.J.H. & Ahsanullah, M. 1982. The signicance of temperature, salinity and zinc as
lethal factors for the mussel Mytilus edulis in a polluted estuary. Marine Biology 68, 135–141.
MARIA BYRNE
32
Crain, C.M., Kroeker, K. & Halpern, B.S. 2008. Interactive and cumulative effects of multiple human stressors
in marine systems. Ecology Letters 11, 1304–1315.
Darszon, A., Guerrero, A., Galindo, B.E., Nishigaki, T. & Wood, C.D. 2008. Sperm-activating peptides in
the regulation of ion uxes, signal transduction and motility. International Journal of Developmental
Biology 52, 595–606.
Davis, M. 2000. The combined effects of temperature and salinity on growth, development and survival for
tropical gastropod veligers of Strombus gigas. Journal of Shellsh Research 19, 883–889.
deRivera, C.E., Hitchcock, G., Teck, G., Steve, B.P., Hines, A.H. & Ruiz, G.M. 2007. Larval development rate
predicts range expansion of an introduced crab. Marine Biology 150, 1275–1288.
Derry, A.M. & Arnott, S.E. 2007. Adaptive reversals in acid tolerance in copepods from lakes recovering from
historical stress. Ecological Applications 17, 1116–1126.
Dinnel, P.A., Link, J.M. & Stober, Q.J. 1987. Improved methodology for a sea-urchin sperm cell bioassay for
marine waters. Archives of Environmental Contamination and Toxicology 16, 23–32.
Doney, S.C., Fabry, V.J., Feely, R.A. & Kleypas, J.A. 2009. Ocean acidication: the other CO2 problem. Annual
Review of Marine Science 1, 169–192.
Doroudi, M.S., Southgate, P.C. & Mayer, R.J. 1999. The combined effects of temperature and salinity on embryos
and larvae of the black-lip pearl oyster, Pinctada margaritifera (Linnaeus). Aquatic Research 30, 271–277.
Dupont, S., Havenhand, J., Thorndyke, W., Peck, L. & Thorndyke, M. 2008. Near-future level of CO2-driven
ocean acidication radically affects larval survival and development in the brittlestar Ophiothrix fragilis.
Marine Ecology Progress Series 373, 285–294.
Dupont, S., Lundve, B. & Thorndyke, M. 2010b. Near future ocean acidication increased growth rate of the
lecithotrophic larvae and juveniles of the sea star Crossaster papposus. Journal of Experimental Zoology
(Molecular Evolution and Development) 314B, 382–389.
Dupont, S., Ortega-Martínez, O. & Thorndyke, M.C. 2010a. Impact of near future ocean acidication on echi-
noderms. Ecotoxicology 19, 440–462.
Edwards, M. & Richardson, A.J. 2004. Impact of climate change on marine pelagic phenology and trophic
mismatch. Nature 430, 881–884.
Egilsdottir, H., Spicer, J.I. & Rundle, S.D. 2009. The effect of CO2 acidied sea water and reduced salinity
on aspects of the embryonic development of the amphipod Echinogammarus marinus (Leach). Marine
Pollution Bulletin 58, 1187–1191.
Ellis, R.P., Bersey, J., Rundle, S.D., Hall-Spencer, J. & Spicer, J.I. 2009. Subtle but signicant effects of CO2
acidied sea water on embryos of the intertidal snail, Littorina obtusata. Aquatic Biology 5, 41–48.
Ericson, J.A., Lamare, M.D., Morley, S.A. & Barker, M.F. 2010. The response of two ecologically important
Antarctic invertebrates (Sterechinus neumayeri and Parborlasia corrugatus) to reduced seawater pH:
Effects on fertilisation and embryonic development. Marine Biology 157, 2689–2702.
Ettinger-Epstein, P., Whalan, S., Battershill, C.N. & de Nys, R. 2007. Temperature cues gametogenesis and
larval release in a tropical sponge. Marine Biology 153, 171–178.
Evans, J.P., García-González, F. & Marshall, D.J. 2007. Sources of genetic and phenotypic variance in fertiliza-
tion rates and larval traits in a sea urchin. Evolution 61, 2832–2838.
Evans, J.P. & Marshall, D.J. 2005. Male-by-female interactions inuence fertilization success and mediate the
benets of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59, 106–112.
Fabry, V.J., McClintock, J.B., Mathis, J.T. & Grebmeier, J.M. 2009. Ocean acidication at high latitudes: the
bellwether. Oceanography 22, 160–171.
Fabry, V.J., Seibel, B.A., Feely, R.A. & Orr, J.C. 2008. Impacts of ocean acidication on marine fauna and
ecosystem processes. Journal of Marine Science 65, 414–432.
Feely, R.A., Doney, S.C. & Cooley, S.R. 2009. Ocean acidication: present conditions and future changes in a
high-CO2 world. Oceanography 22, 36–47.
Feely, R.A., Sabine, C.L., Lee, K., Berelson, W., Kleypas, J., Fabry, V.J. & Millero, F.J. 2004. Impact of anthro-
pogenic CO2 on the CaCO3 system in the oceans. Science 305, 362–366.
Figueira, W.F. & Booth, D.J. 2010. Increasing ocean temperatures allow tropical shes to survive over winter
in temperate waters. Global Change Biology 16, 506–516.
Findlay, H.S., Kendall, M.A., Spicer, J.I., Turley, C. & Widdicombe, S. 2008. A novel microcosm system for
investigating the impacts of elevated carbon dioxide and temperature on intertidal organisms. Aquatic
Biology 3, 51–62.
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
33
Findlay, H.S., Kendall, M.A., Spicer, J.I. & Widdicombe, S. 2010a. Post-larval development of two intertidal
barnacles at elevated CO2 and temperature. Marine Biology 157, 725–735.
Findlay, H.S., Kendall, M.A., Spicer, J.I. & Widdicombe, S. 2010b. Relative inuences of ocean acidication
and temperature on intertidal barnacle post-larvae at the northern edge of their geographic distribution.
Estuarine Coastal and Shelf Science 86, 675–682.
Fine, M. & Tchernov, D. 2007. Scleractinian coral species survive and recover from decalcication. Science
315, 1811.
Folt, C.L., Chen, C.Y., Moore, M.V. & Burnaford, J. 1999. Synergism and antagonism among multiple stres-
sors. Limnology and Oceanography 44, 864–877.
Foo, S.A. 2010. The impact of climate change stressors on the development of calcifying and non-calcifying
echinoderm larvae and potential for adaptive change. BSc Honours Thesis, University of Sydney.
Fujisawa, H. 1989. Differences in temperature dependence of early development of sea urchins with different
growing seasons. Biological Bulletin (Woods Hole) 176, 96–102.
Fujisawa, H. 1993. Temperature sensitivity of a hybrid between two species of sea urchin differing in thermo-
tolerance. Development Growth and Differentiation 35, 395–401.
Fujisawa, H. 1995. Variation in embryonic temperature sensitivity among groups of the sea urchin, Hemicentrotus
pulcherrimus, which differ in their habitats. Zoological Science 12, 583–589.
Fujisawa, H. & Shigei, M. 1990. Correlation of embryonic temperature sensitivity of sea urchins with spawning
season. Journal of Experimental Marine Biology and Ecology 136, 123–139.
Galletly, B.C., Blows, M.W. & Marshall, D.J. 2007. Genetic mechanisms of pollution resistance in a marine
invertebrates. Ecological Applications 17, 2290–2297.
Gaston, K.J. & Spicer, J.I. 1998. Do upper thermal tolerances differ in geographically separated populations
of the beach ea Orchestia gammarellus (Crustacea: Amphipoda)? Journal of Experimental Marine
Biology and Ecology 229, 265–276.
Gazeau, F., Quiblier, C., Jansen, J., Gattuso, J-P., Middelburg, J.J. & Heip, C.H.R. 2007. Impact of elevated CO2
on shellsh calcication. Geophysical Research Letters 34, L07603.
Gienapp, P., Teplitsky, C., Alho, J.A., Mills, A. & Merilä, J. 2008. Climate change and evolution: disentangling
environmental and genetic responses. Molecular Ecology 17, 167–178.
Giese, A.C. & Pearse, J.S. 1974. Introduction: general principles. In Reproduction of Marine Invertebrates,
Volume 1. Acoelomate and Pseudocoelomate Metazoans, A.C. Giese & J.S. Pearse (eds). New York:
Academic Press, 1–49.
Gillooly, J.F., Charnov, E.L., West, G.B., Savage, V.M. & Brown, J.H. 2002. Effects of size and temperature on
developmental time. Nature 417, 70–73.
Gilroy, A. & Edwards, S.J. 1998. Optimum temperature for growth of Australian abalone: preferred tempera-
ture and critical; thermal maximum four blacklip abalone, Haliotis rubra (Leach), and greenly abalone,
Haliotis lavegiata (Leach). Aquaculture Research 2, 481–485.
Gooding, R.A., Harley, C.D.G. & Tang, E. 2009. Elevated water temperature and carbon dioxide concentration
increase the growth of a keystone echinoderm. Proceedings of the National Academy of Sciences of the
United States of America 106, 9316–9321.
Gosselin, L.A. & Qian P.-Y. 1997. Juvenile mortality in benthic marine invertebrates. Marine Ecology Progress
Series 146, 264–282.
Green, M.A., Jones, M.E., Boudreau, C.L., Moore, R.L. & Westman, B.A. 2004. Dissolution mortality of juve-
nile bivalves in coastal marine deposits. Limnology and Oceanography 49, 727–734.
Greenwood, P.J. & Bennett, T. 1981. Some effects of temperature-salinity combinations on the early develop-
ment of the sea urchin Parachinus angulosus (Leske). Fertilization. Journal of Experimental Marine
Biology and Ecology 51, 119–131.
Gutowska, M.A., Melzner, F., Langenbuch, M., Bock, C., Claireaux, G. & Pörtner, H.O. 2010a. Acid-base
regulatory ability of the cephalopod (Sepia ofcinalis) in response to environmental hypercapnia. Journal
of Comparative Physiology B 180, 323–335.
Gutowska, M.A., Melzner, F., Pörtner, H.O. & Meier, S. 2010b. Cuttlebone calcication increases during expo-
sure to elevated seawater pCO2in the cephalopod Sepia ofcinalis. Marine Biology 157, 1653–1663.
Gutowska, M.A., Pörtner, H.O. & Melzner, F. 2008. Growth and calcication in the cephalopod Sepia ofcina-
lis under elevated seawater pCO2. Marine Ecology Progress Series 373, 303–309.
Hadeld, M.G. & Strathmann, M.F. 1996. Variability, exibility and plasticity in life histories of marine inver-
tebrates. Oceanologica Acta 19, 323–324.
MARIA BYRNE
34
Hale, R., Calosi, P., McNeill, L., Mieszkowska, N. & Widdicombe, S. 2011. Predicted levels of future ocean
acidication and temperature rise could alter community structure and biodiversity in marine benthic
communities. Oikos DOI: 10.1111/j.1600-0706.2010.
Hall-Spencer, J.M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M., Turner, S.M., Rowley, S.J.,
Tedesco, D. & Buia, M.C. 2008. Volcanic carbon dioxide vents reveal ecosystem effects of ocean acidi-
cation. Nature 454, 96–99.
Halpern, B.S., Walbridge, S., Selkoe, K.A., Kappel, C.V., Micheli, F., D’Agrosa, D., Bruno, J.F., Casey,
K.S., Ebert, C. & Fox, H.E. 2008. A global map of human impact on marine ecosystems. Science 319,
948–952.
Hamdoun, A. & Epel, D. 2007. Embryo stability and vulnerability in an always changing world. Proceedings
of the National Academy of Sciences of the United States of America 104, 1745–1750.
Hammond, L.M. & Hofmann, G.E. 2010. Thermal tolerance of Strongylocentrotus purpuratus early
life history stages: mortality, stress-induced gene expression and biogeographic patterns. Marine
Biology doi:10.1007/s00227-010-1528-z.
Harley, C.D.G., Hughes, A.R., Hultgren, K.M., Miner, B.G., Sorte, C.J.B., Thornber, C.S., Rodriguez, L.F.,
Tomanek, L. & Williams, S.L. 2006. The impacts of climate change in coastal marine systems. Ecology
Letters 9, 228–241.
Harley, C.D.G. & Paine, R.T. 2009. Contingencies and compounded rare perturbations dictate sudden distribu-
tional shifts during periods of gradual climate change. Proceedings of the National Academy of Sciences
of the United States of America 106, 11172–11176.
Hart, M.W. & Scheibling, R.E. 1988. Heat waves, baby booms and the destruction of kelp beds by sea urchins.
Marine Biology 99, 167–176.
Havenhand, J.N., Butler, F.R., Thorndyke, M.C. & Williamson, J.E. 2008. Near-future levels of ocean acidica-
tion reduce fertilization success in a sea urchin. Current Biology 18, 651–652.
Havenhand, J.N. & Schlegel, P. 2009. Near-future levels of ocean acidication do not affect sperm motility and
fertilization kinetics in the oyster Crassostrea gigas. Biogeosciences Discussions 6, 4573–4586.
Hay, G.C., Richardson, A.J. & Robinson, C. 2005. Climate change and marine plankton. Trends in Ecology and
Evolution 20, 338–344.
Hellberg, M.E., Balch, D.P. & Roy, K. 2001. Climate-driven range expansion and morphological evolution in a
marine gastropod. Science 292, 1707–1710.
Helmuth, B., Mieszkowska, N., Moore P. & Hawkins, S. 2006. Living on the edge of two changing worlds:
forecasting the responses of rocky intertidal ecosystems to climate change. Annual Review of Ecology
Evolution and Systematics 37, 373–404.
Hendriks, I.E., Duarte, C.M. & Álvarez, A. 2010. Vulnerability of marine biodiversity to ocean acidication: a
meta-analysis. Estuarine Coastal and Shelf Science 86, 157–164.
Hernández, J.C., Clemente, S., Girard, D., Pérez-Ruzafa, A. & Brito, A. 2010. Effect of temperature on settlement
and postsettlement survival in a barrens-forming sea urchin. Marine Ecology Progress Series 413, 69–80.
Heyward, A.J. & Negri, A.P. 2010. Plasticity of larval pre-competency in response to temperature: observations
on multiple broadcast spawning coral species. Coral Reefs 29, 631–636.
Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greeneld, P., Gomez, E., Harvell, C.D., Sale,
P.F., Edwards, A.J., Caldeira, K., Knowlton, N., Eakin, C.M., Iglesias-Prieto, R., Muthiga, N., Bradbury,
R.H., Dubi, S. & Hatziolos, M.E. 2007. Coral reefs under rapid climate change and ocean acidication.
Science 318, 1737–1742.
Hoegh-Guldberg, O. & Pearse, J.S. 1995. Temperature, food availability, and the development of marine inver-
tebrate larvae. American Zoologist 35, 415–425.
Hoffmann, A.A. & Merilä, J. 1999. Heritable variation and evolution under favourable and unfavourable condi-
tions. Trends in Ecology and Evolution 14, 96–101.
Hofmann, G.E. & Todgham, A.E. 2010. Living in the now: physiological mechanisms to tolerate a rapidly
changing environment. Annual Review of Physiology 72, 127–45.
Hughes, T.P., Baird, A.H., Bellwood, D.R., Card, M., Connolly, S.R., Folke, C., Grosberg, R., Hoegh-Guldberg,
O., Jackson, J.B.C., Kleypas, J., Lough, J.M., Marshall, P., Nyström, M., Palumbi, S.R., Pandol, J.M.,
Rosen, B. & Roughgarden, J. 2003. Climate change, human impacts and the resilience of coral reefs.
Science 310, 929–933.
Hunt, M.W. & Scheibling, R.E. 1997. Role of early post-settlement mortality in recruitment of benthic marine
invertebrates. Marine Ecology Progress Series 155, 269–301.
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
35
Intergovernmental Panel on Climate Change (IPCC). 2007. Climate Change 2007: The Fourth Assessment
Report of the Intergovernmental Panel on Climate Change (IPCC). Cambridge, UK: Cambridge Univer-
sity Press.
Jackson, J.B.C. & Johnson, K.G. 2000. Life in the last few million years. Paleobiology 26, 221–235.
Jeffery, C.H., Emlet, R.B. & Littlewood, D.T.J. 2003. Phylogeny and evolution of developmental mode in tem-
nopleurid echinoids. Molecular Phylogenetics and Evolution 28, 99–118.
Johnson, C.H., Clapper, D.L., Winkler, M.M., Lee, H.C. & Epel, D. 1983. A volatile inhibitor immobilizes sea
urchin sperm in semen by depressing the intracellular pH. Developmental Biology 98, 493–501.
Johnson, J.D. & Epel, D. 1975. Relationship between release of surface proteins and metabolic activation of
sea urchin eggs at fertilization. Proceedings of the National Academy of Sciences of the United States of
America 72, 4474–4478.
Johnson, L.G. & Babcock, R.C. 1994. Temperature and the larval ecology of the crown-of-thorns starsh,
Acanthaster planci. Biological Bulletin (Woods Hole) 168, 419–431.
Jones, W.J., Mieszkowska, N. & Wethey, D. 2009. Linking thermal tolerances and biogeography: Mytilus edulis
(L.) at its southern limit on the east coast of the United States. Biological Bulletin (Woods Hole) 217,
73–85.
Kiessling, W. & Simpson, C. 2011. On the potential for ocean acidication to be a general cause of ancient reef
crises. Global Change Biology 17, 56–67.
Kinne, O. 1970. Invertebrates. Temperature effects. In Marine Ecology. Environmental Factors, Part 1 Volume 1,
O. Kinne (ed.). Chichester, UK: Wiley-Interscience, 407–514.
Kirby, R.E., Beaugrand, G., Lindley, J.A., Richardson, A.J., Edwards, M. & Reid, P.C. 2007. Climate effects
and benthic-pelagic coupling in the North Sea. Marine Ecology Progress Series 330, 31–38.
Kleypas, J.A., Buddemeier, R.W., Eakin, C.M., Gattusso, J.P., Guinotte, J., Hoegh-Guldberg, O.,
Iglesias-Prieto, T., Jokiel, J.P., Langdon, C., Skirving, W. & Strong, A.E. 2005. Comment on ‘Coral
reef calcication and climate change: The effect of ocean warming’. Geophysical Research Letters
32, L08601.
Kleypas, J.A. & Yates, K.K. 2009. Coral reefs and ocean acidication. Oceanography 22, 108–117.
Knutzen, J. 1981. Effects of decreased pH on marine organisms. Marine Pollution Bulletin 12, 25–29.
Kroeker, J.J., Kordas, R.L., Crim, R.N., & Singh, G.G. 2010. Meta-analysis reveals negative yet variable effects
of ocean acidication on marine organisms. Ecology Letters 13, 1419–1434.
Kuo, E.S.L. & Sanford, E. 2009. Geographic variation in the upper thermal limits of an intertidal snail: implica-
tions for climate envelope models. Marine Ecology Progress Series 388, 137–146.
Kupriyanova, E.K. & Havenhand, J.N. 2005. Effects of temperature on sperm swimming behaviour, respira-
tion and fertilization success in the serpulid polychaete, Galeolaria caesepitosa (Annelida: Serpulidae).
Invertebrate Reproduction and Development 48, 7–17.
Kurihara, H. 2008. Effects of CO2-driven ocean acidication on the early development stages of invertebrates.
Marine Ecology Progress Series 373, 275–284.
Kurihara, H. & Ishimatsu, A. 2008. Effects of high CO2 seawater on the copepod (Acartia tsuensis) through all
life stages and subsequent generations. Marine Pollution Bulletin 56, 1086–1090.
Kurihara, H., Kato, S. & Ishimatsu, A. 2007. Effects of increased seawater pCO2 on early development of the
oyster Crassotrea gigas. Aquatic Biology 1, 91–98.
Kurihara, H., Kato, S. & Ishimatsu, A. 2008a. Effects of elevated pCO2 on early development in the mussel
Mytilus galloprovincialis. Aquatic Biology 4, 225–233.
Kurihara, H., Matsui, M., Furukawa, H., Hayashi, M. & Ishimatsu, A. 2008b. Long-term effects of predicted
future seawater CO2 conditions on the survival and growth of the marine shrimp Palaemon pacicus.
Journal of Experimental Marine Biology and Ecology 367, 41–46.
Kurihara, H., Shimode, S. & Shirayama, Y. 2004. Effects of raised CO2 concentration on the egg production
rate and early development of two marine copepods (Acartia steueri and Acartia erythraea). Marine
Pollution Bulletin 49, 721–727.
Kurihara, H. & Shirayama, Y. 2004. Effects of increased atmospheric CO2 on sea urchin early development.
Marine Ecology Progress Series 274, 161–169.
Lamare, M.D. & Barker, M.F. 1999. In situ estimates of larval development and mortality in the New Zealand
sea urchin Evechinus chloroticus (Echinodermata: Echinoidea). Marine Ecology Progress Series 180,
197–211.
MARIA BYRNE
36
Lee, C.H., Ryu, T.K. & Choi, J.W. 2004. Effects of water temperature on embryonic development in the north-
ern Pacic asteroid, Asterias amurensis, from the southern coast of Korea. Invertebrate Reproduction and
Development 45, 109–116.
Lera, S., Maccia, S. & Pellegrini, D. 2006. Standardizing the methodology of the sperm cell test with
Paracentrotus lividus. Environmental Monitoring and Assessment 122, 101–109.
Lester, S.E., Tobin, E.D. & Behrens, M.D. 2007. Disease dynamics and the potential role of thermal stress in
the sea urchin, Strongylocentrotus purpuratus. Canadian Journal of Fisheries and Aquatic Sciences 64,
314–323.
Levinton, J.S., Suatoni, L., Wallace, W.P., Junkins, R., Kelaher, B.P. & Allen, B.J. 2003. Rapid loss of geneti-
cally-based resistance to metals, following the cleanup of a Superfund site. Proceedings of the National
Academy of Sciences of the United States of America 100, 9889–9891.
Levitan, D.R. & Ferrell, D.L. 2006. Selection on gamete recognition proteins depends on sex, density, and
genotype frequency. Science 312, 267–269.
Lewis, C., Olive, P.J.W., Bentley, M.G. & Watson, G. 2002. Does seasonal reproduction occur at the opti-
mal time for fertilization in the polychaetes Arenicola marina L. and Nereis virens Sars? Invertebrate
Reproduction and Development 41, 61–71.
Ling, S.D., Johnson, C.R., Ridgway, K., Hobday, A.J. & Haddon, M. 2009. Climate-driven range extension of
a sea urchin: inferring future trends by analysis of recent population dynamics. Global Change Biology
15, 719–731.
Lucas, T., Macbeth, M., Degnan, S.M., Knibb, W. & Degnan, B.M. 2006. Heritability estimates for growth in the
tropical abalone Haliotis asinina using microsatellites to assign parentage. Aquaculture 259, 146–152.
Luquet, G. & Marin, F. 2004. Biomineralisations in crustaceans: storage strategies. Comptes Rendus
Paleoevolution 3, 515–534.
MacInnes, J.R. & Calabrese, A. 1979. Combined effect of salinity, temperature and copper on embryos and
early larvae of the American oyster, Crassostrea virginica. Archives of Environmental Contamination
and Toxicology 8, 553–562.
Mangum, C.P. & Shick, J. 1972. The pH of body uids of marine invertebrates. Comparative Biochemistry and
Physiology 42, 693–697.
Manno, C., Sandrini, S., Tositti, L. & Accornero, A. 2007. First stages of degradation of Limacina helicina
shells observed above aragonite chemical lysocline in Terra Nova Bay (Antarctica). Journal of Marine
Systems 68, 91–102.
Marshall, D.J., Santos, J.H., Leung, K.M.Y. & Chak, W.H. 2008. Correlations between gastropod shell dissolu-
tion and water chemical properties in a tropical estuary. Marine Environmental Research 66, 422–429.
Matear, R.J. & McNeil, B.I. 2006. Comment on ‘Preindustrial to modern interdecadal variability in coral reef
pH’. Science 314, 595.
Matsui, T., Nishiyama, I., Hino, A. & Hoshi, M. 1986. Intracellular pH changes of starsh sperm upon the
acrosome reaction. Development Growth and Differentiation 28, 359–368.
Mayor, D.J., Matthew, C., Cook, K., Zuur, A.F. & Hay S. 2007. CO2-induced acidication affects hatching suc-
cess in Calanus nmarchicus. Marine Ecology Progress Series 350, 91–97.
McClintock, J.B., Angus, R.A., Mcdonald, M.R., Amsler, C.D., Catledge, S.A. & Vohra, Y.K. 2009. Rapid
dissolution of shells of weakly calcied Antarctic benthic macroorganisms indicate high vulnerability to
ocean acidication. Antarctic Science 21, 449–56.
McDonald, K. 2004. Patterns in early embryonic motility: effects of size and environmental temperature on
vertical velocities of sinking and swimming echinoid blastulae. Biological Bulletin (Woods Hole) 207,
93–102.
McDonald, M.R., McClintock, J.B., Amsler, C.D., Rittschof, D., Angus, R.A., Orihuela, B. & Lutostanski,
K. 2009. Effects of ocean acidication over the life history of the barnacle Amphibalanus amphitrite.
Marine Ecology Progress Series 385, 179–187.
McLusky, D.S., Bryant, V. & Campbell, R. 1986. The effects of temperature and salinity on the toxicity of
heavy metals to marine and estuarine invertebrates. Oceanography and Marine Biology Annual Review
24, 481–520.
McNeil, B.I. & Matear, R. 2008. Southern Ocean acidication: a tipping point at 450-ppm atmospheric CO2.
Proceedings of the National Academy of Sciences of the United States of America 105, 18860–18864.
McNeil, B.I., Matear, R.J. & Barnes, D. 2004. Coral reef calcication and climate change: the effect of ocean
warming. Geophysical Research Letters 31, L22309,
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
37
Melzner, F., Gutowska, M.A., Langenbuch, M., Dupont, S., Lucassen, M., Thorndyke, M.C., Bleich, M. &
Pörtner, H.-O. 2009. Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-
adaptation through lifestyle and ontogeny? Biogeosciences 6, 2313–2331.
Metzger, R., Sartoris, F.J., Lagenbuch, M. & Pörtner H.O. 2007. Inuence of elevated CO2 concentrations on
thermal tolerance of the edible crab Cancer pagurus. Journal of Thermal Biology 32, 144–151.
Michaelidis, B., Ouzounis, C., Paleras, A. & Portner, H.O. 2005. Effects of long-term moderate hypercapnia on
acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology Progress
Series 293, 109–118.
Miles, H., Widdicombe, S., Spicer, J.I. & Hall-Spencer, J. 2007. Effects of anthropogenic seawater acidication
on acid-base balance in the sea urchin Psammechinus miliaris. Marine Pollution Bulletin 54, 89–96.
Miller, A.W., Reynolds, A.C., Sobrino, C. & Riedel, G.F. 2009. Shellsh face uncertain futures in high ρCO2
world: inuence of acidication in oyster larvae calcication and growth in estuaries. PLoS ONE 4, 108.
Miller, R.L. 1985. Demonstration of sperm chemotaxis in echinodermata: Asteroidea, Holothuroidea,
Ophiuroidea. Journal of Experimental Zoology 234, 383–414.
Miller, R.L. 1997. Specicity of sperm chemotaxis among great barrier reef shallow-water holothurians and
ophiuroids. Journal of Experimental Zoology 279, 189–200.
Millero, F.J., Woosley, R., DiTrolio, B. & Waters, J. 2009. Effect of ocean acidication on the speciation of
metals in seawater. Oceanography 22, 72–85.
Mita, M., Hino, A. & Yasumasu, I. 1984. Effect of temperature on interaction between eggs and spermatozoa
of sea urchin. Biological Bulletin (Woods Hole) 166, 68–77.
Montes-Hugo, M., Doney, S.C., Ducklow, H.W., Fraser, W., Martinson, D., Stammerjohn, S.E. & Schoeld,
O. 2009. Recent changes in phytoplankton communities associated with rapid regional climate change
along the Western Antarctic Peninsula. Science 323, 1470–1473.
Moore, P.J., Thompson, R.C. & Hawkins, S.J. 2010. Phenological changes in intertidal con-specic gastropods
in response to climate warming. Global Change Biology doi:10.1111/j.1365-2486.2010.02270.x.
Morita, M., Kitamura, M., Nakajima, A., Sri Susilo, E., Takemura, A. & Okuno, M. 2009. Regulation of sperm
agellar motility activation and chemotaxis caused by egg-derived substance(s) in sea cucumber. Cell
Motility and the Cytoskeleton 66, 202–214.
Morita, M., Nishikawa, A., Nakajima, A., Iguchi, A., Sakai, K., Takemura A. & Okuno, M. 2006. Eggs regulate
sperm agellar motility initiation, chemotaxis and inhibition in the coral Acropora digitifera, A. gem-
mifera and A. tenuis. Journal of Experimental Biology 209, 4574–4579.
Morita, M., Suwa, R., Iguchi, A., Nakamura, M., Shimada, K., Sakai, K. & Suzuki, A. 2010. Ocean acidica-
tion reduces sperm agellar motility in broadcast spawning reef invertebrates. Zygote 18, 103–107.
Morris, S. & Taylor, A.C. 1983. Diurnal and seasonal variation in physico-chemical conditions within intertidal
rock pools. Estuarine Coastal and Shelf Science 17, 339–355.
Moy, A.D., Howard, W.R., Bray, S.G. & Trull, T.W. 2009. Reduced calcication in modern Southern Ocean
planktonic foraminifera. Nature Geoscience 2, 276–280.
Mueter, F.J. & Litzow, M.A. 2009. Sea ice retreat alters the biogeography of the Bearing Sea continental shelf.
Ecological Applications 18, 309–320.
Munday, P.L., Dixson, D.L., Donelson, J.M., Jones, G.P., Pratchett, M.S., Devitsina, K.P. & Doving, K.B. 2009.
Ocean acidication impairs olfactory discrimination and homing ability of a marine sh. Proceedings of
the National Academy of Sciences of the United States of America 106, 1848–1852.
Nakamura, M., Ohki, S., Suzuki, A. & Sakai, K. 2011. Coral larvae under ocean acidication: survival, metabo-
lism and metamorphosis. PLoSOne 6, e14521.
Negri, A.P., Marshall, P.A. & Heyward, A.J. 2007. Differing effects of thermal stress on coral fertilization and
early embryogenesis in four Indo Pacic species. Coral Reefs 26, 759–763.
Nguyen, H.D., Byrne, M., & Thompson, M. 2011. Hsp70 expression in the south-eastern Australian sea urchins
Heliocidaris erythrogramma and H. tuberculata. In Echinoderms in a Changing World (C. Johnson ed.).
Balkema, Rotterdam, in press.
Nienhuis, S., Palmer, A. & Harley, C. 2010. Elevated CO2 affects shell dissolution rate but not calcication rate
in a marine snail. Proceedings of the Royal Society B 277, 2553–2558.
O’Connor, C. & Mulley, J.C. 1977. Temperature effects on periodicity and embryology, with observations on
the population genetics, of the aquacultural echinoid Heliocidaris tuberculata. Aquaculture 12, 99–114.
MARIA BYRNE
38
O’Connor, M.I., Bruno, J.F., Gaines, S.D., Halpern, B.S., Lester, S.E., Kinlan, B.P. & Weiss, J.M. 2007.
Temperature control of larval dispersal and the implications for marine ecology, evolution, and con-
servation. Proceedings of the National Academy of Sciences of the United States of America 104,
1266–1271.
O’Connor, M.I., Piehler, M.F., Leech, D.M., Anton, A. & Bruno, J.F. 2009. Warming and resource availability
shift food web structure and metabolism. PLoS Biology 7, 1–5.
O’Donnell, M.J., Hammond, L.M. & Hoffman, G.E. 2009. Predicted impact of ocean acidication on a marine
invertebrate: elevated CO2 alters response to thermal stress in sea urchin larvae. Marine Biology 156,
439–446.
O’Donnell, M.J., Todgham, A.E., Sewell, M.A., LaTisha, M.H., Ruggiero, K., Fangue, N.A., Zippay, M.L. &
Hofmann, G.E. 2010. Ocean acidication alters skeletogenesis and gene expression in larval sea urchins.
Marine Ecology Progress Series 398, 157–171.
Olive, P.J.W. 1995. Annual breeding cycles in marine invertebrates and environmental temperature: probing the
proximate and ultimate causes of reproductive synchrony. Journal of Thermal Biology 20, 79–90.
Orr, J.C., Fabry, V.J., Aumont, O., Bopp, L., Doney, S.C., Feely, R.A., Gnanadesikan, A., Gruber, N., Ishida, A.,
Joos, F., Key, R.M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R.G.,
Plattner, G.-K., Rodgers, K.B., Sabine, C.L., Sarmiento, J.L., Schlitzer, R., Slater, R.D., Totterdell, I.J.,
Weirig, M.-F., Yamanaka, Y. & Yool A. 2005. Anthropogenic ocean acidication over the twenty-rst
century and its impact on calcifying organisms. Nature 437, 681–686.
Palmer, A.R. 1994. Temperature sensitivity, rate of development, and time to maturity: geographic variation in
laboratory reared Nucella and a cross-phyletic overview. In Reproduction and Development of Marine
Invertebrates, W.H. Wilson et al. (eds). Baltimore: Johns Hopkins University Press, 177–194.
Palumbi, S.R. 1999. All males are not created equal: fertility differences depend on gamete recognition poly-
morphisms in sea urchins. Proceedings of the National Academy of Sciences of the United States of
America 96, 12632–12637.
Parker, L.M., Ross, P.M. & O’Connor, W.A. 2009. The effect of ocean acidication and temperature on the
fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850).
Global Change Biology 15, 2123–2136.
Parker, L.M., Ross, P.M. & O’Connor, W.A. 2010. Comparing the effect of elevated pCO2 and temperature on
the fertilization and early development of two species of oysters. Marine Biology 157, 2435–2452.
Pechenik, J.A. 1987. Environmental inuences on larval survival and development. In Reproduction of Marine
Invertebrates, A.C. Giese & J.S. Pearse (eds). New York: Academic Press, 551–608.
Pechenik, J.A. 1999. On the advantages and disadvantages of larval stages in benthic marine invertebrate life
cycles. Marine Ecology Progress Series 177, 269–297.
Peck, L.S. 2005. Prospects for survival in the Southern Ocean: vulnerability of benthic species to temperature
change. Antarctic Science 17, 497–507.
Philippart, C.J.M., van Aken, H.M., Beukema, J.J., Bos, O.G., Cadee, G.C. & Dekker, R. 2003. Climate-related
changes in recruitment of the bivalve Macoma balthica. Limnology and Oceanography 48, 2171–2185.
Poloczanska, E.S., Babcock, R.C., Butler, A., Hobday, A.J., Hoegh-Guldberg, O., Kunz, T.J., Matear, R., Milton,
D.A., Okey, T.A. & Richardson, A.J. 2007. Climate change and Australian marine life. Oceanography
and Marine Biology Annual Review 45, 407–478.
Porter, S.M. 2007. Sea water chemistry and early carbonate biomineralization. Science 316, 1302.
Pörtner, H.O. 2008. Ecosystem effects of ocean acidication in times of ocean warming: a physiologist’s view.
Marine Ecology Progress Series 373, 203–217.
Pörtner, H.O. 2010. Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-
related stressor effects in marine ecosystems. Journal of Experimental Biology 213, 881–893.
Pörtner, H.O. & Knust, R. 2007. Climate change affects marine shes through the oxygen limitation of thermal
tolerance. Science 315, 95–97.
Pörtner, H.O., Langenbuch, M. & Michaelidis, B. 2005. Synergistic effects of temperature extremes, hypoxia,
and increases in CO2 on marine animals: from Earth history to global change. Journal of Geophysical
Research 110, C09S10.
Pörtner, H.O., Langenbuch, M. & Reipschläger, A. 2004. Biological impact of elevated ocean CO2 concentra-
tions: lessons from animal physiology and earth history. Journal of Oceanography 60, 705–718.
Przeslawski, R. 2004. A review of the effects of environmental stress on embryonic development within inter-
tidal gastropod egg masses. Molluscan Research 24, 43–63.
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
39
Przeslawski, R., Ahyong, S., Byrne, M., Worheide, G. & Hutchings, P. 2008. Beyond corals and sh: the
effects of climate change on non-coral benthic invertebrates of tropical reefs. Global Change Biology
14, 2773–2795.
Przeslawski, R. & Davis, A.R. 2007. Does spawning behavior minimize exposure to environmental stressors
for encapsulated gastropod embryos on rocky shores? Marine Biology 152, 991–1002.
Przeslawski, R., Davis, A.R. & Benkendorff, K. 2005. Synergies, climate change and the development of rocky
shore invertebrates. Global Change Biology 11, 515–522.
Punzo, F. 1977. The pH of body uids from marine intertidal invertebrates. Journal of Experimental Marine
Biology and Ecology 30, 327–331.
Putnam, H.M., Edmunds, P.J. & Fan, T.Y. 2008. Effect of temperature on the settlement choice and photophysi-
ology of larvae from the reef coral Stylophora pistillata. Biological Bulletin (Woods Hole) 215, 135–142.
Putnam, H.M., Edmunds, P.J. & Fan, T.Y. 2010. Effect of uctuating thermal regime on adult and larval reef
corals. Invertebrate Biology 129, 199–209.
Raff, R.A. & Byrne, M. 2006. The active evolutionary lives of echinoderm larvae. Heredity 97, 244–252.
Rahman, S., Tsuchiya, M. & Uehara, T. 2009. Effects of temperature on hatching rate, embryonic development
and early larval survival of the edible sea urchin, Tripneustes gratilla. Biologia 64, 768–775.
Ramofaa, C., Byrne, M. & Battaglene, S.C. 2003. Development of the commercial sea cucumbers, Holothuria
scabra, H. fuscogilva and Actinopyga mauritiana: larval structure and growth. Marine and Freshwater
Research 54, 657–667. Also CSIRO http://www.publish.csiro.au/nid/126/paper/MF02145.htm
Randall, C.J. & Szmant, A.M. 2009a. Elevated temperature affects development, survivorship, and settlement of
the Elkhorn Coral, Acropora palmata (Lamarck 1816). Biological Bulletin (Woods Hole) 217, 269–282.
Randall, C.J. & Szmant, A.M. 2009b. Elevated temperature reduces survivorship and settlement of the larvae of
the Caribbean scleractinian coral, Favia fragum (Esper). Coral Reefs 28, 537–545.
Range, P., Chícharo, M.A., Ben-Hamadou, R., Piló, D., Matias, D., Joaquim, S., Oliveira, A.P. & Chícharo,
L. 2011. Calcication, growth and mortality of juvenile clams Ruditapes decussatus under increased
pCO2 and reduced pH: variable responses to ocean acidication at local scales? Journal of Experimental
Marine Biology and Ecology 396, 177–184.
Reitzel, A.M., Miner, B.G. & McEdward, L.R. 2004. Relationships between spawning date and larval develop-
ment time for benthic marine invertebrates: a modelling approach. Marine Ecology Progress Series 280,
13–23.
Reuter, K.E., Lotterhos, K.E., Crim, R.N., Thompson, C.A. & Harley, C.D.G. 2011. Elevated pCO2 increases
sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrous franciscanus. Global
Change Biology 17, 163–171.
Richardson, A.J. 2008. In hot water: zooplankton and climate change. ICES Journal of Marine Science 65,
279–295.
Richardson, A.J., McKinnon, D. & Swadling, K.M. 2009. Zooplankton. In A Marine Climate Change Impacts and
Adaptation Report Card for Australia 2009, E.S. Poloczanska et al. (eds). NCCARF Publication 05/09.
Ridgway, K.R. 2007. Long-term trend and decadal variability of the southward penetration of the East Australian
Current. Geophysical Research Letters 34, L13613.
Ries, J.B., Cohen, A.L. & McCorkle, D.C. 2009. Marine calciers exhibit mixed responses to CO2-induced
ocean acidication. Geology 37, 1131–1134.
Riffell, J.A., Krug, P.J. & Zimmer, R.K. 2002. Fertilization in the sea: the chemical identity of an abalone sperm
attractant. Journal of Experimental Biology 205, 1439–1450.
Ringwood, A.H. 1992. Comparative sensitivity of gametes and early developmental stages of a sea urchin
species (Echinometra mathaei) and a bivalve species (Isognomon californicum) during metal exposures.
Archives of Environmental Contamination and Toxicology 22, 288–295.
Ringwood, A.H. & Keppler, C.J. 2002. Water quality variation and clam growth: is pH really a non-issue in
estuaries? Estuaries 25, 910–907.
Riveros, A., Zuñiga, M., Larrain, A. & Becerra, J. 1996. Relationships between fertilization of the southeastern
Pacic sea urchin Arbacia spatuligera and environmental variables in polluted coastal waters. Marine
Ecology Progress Series 134, 159–169.
Rodolfo-Metalpa, R., Lombardi, C., Cocito, S., Hall-Spencer, J.M. & Gambi, M.C. 2010. Effects of ocean
acidication and high temperatures on the bryozoan Myriapora truncata at natural CO2 vents. Marine
Ecology doi: 10.1111/j.1439-0485.2009.00354.x.
MARIA BYRNE
40
Roller, R.A. & Stickle, W.B. 1993. Effects of temperature and salinity acclimations of adults on larval sur-
vival, physiology, and early development of Lytechinus variegatus (Echinodermata: Echinoidea). Marine
Biology 116, 583–591.
Rosa, R. & Seibel, B.A. 2008. Synergistic effects of climate-related variables suggest future physiological
impairment in a top oceanic predator. Proceedings of the National Academy of Sciences of the United
States of America 105, 20776–20780.
Rumrill, S.S. 1990. Natural mortality of marine invertebrate larvae. Ophelia 32, 163–198.
Rupp, J.H. 1973. Effects of temperature on fertilization and early cleavage of some tropical echinoderms, with
emphasis on Echinometra mathaei. Marine Biology 23, 183–189.
Sagarin, R.D., Barry, J.P., Gilman, S.E. & Baxter, C.H. 1999. Climate-related change in an intertidal commu-
nity over short and long time scales. Ecological Monographs 69, 465–490.
Sanford, E. & Kelly, M.W. 2011. Local adaptation in marine invertebrates. Annual Review of Marine Science
3, 509–535.
Schiel, D.R., Steihneck, J.R. & Foster, M.S. 2004. Ten years of induced ocean warming causes comprehensive
changes in marine benthic communities. Ecology 85, 1833–1839.
Schmalenbach, I. & Franke, H.-D. 2010. Potential impact of climate warming on the recruitment of an eco-
nomically and ecologically important species, the European lobster (Homarus gammarus) at Helgoland,
North Sea. Marine Biology 157, 1127–1135.
Schneider, D.W., Stoeckel, J.A., Rehmann, C.R., Blodgett, K.D., Sparks, R.E. & Padilla, D.K. 2003. A developmen-
tal bottleneck in pelagic larvae: implications for spatial population dynamics. Ecology Letters 6, 352–360.
Schoeld, O., Ducklow, H.W., Martinson, D.G., Meridith, M.P., Moline, M.A. & Fraser, W.R. 2010. How do
polar marine ecosystems respond to rapid climate change? Science 328, 1520–1523.
Selvakumaraswamy, P. & Byrne, M. 2000. Reproduction, spawning and development in f5 ophiuroids from
Australia and New Zealand. Invertebrate Biology 119, 394–402.
Sewell, M.A. & Hofmann, G.E. 2011. Antarctic echinoids and climate change: a major impact on brooding
forms. Global Change Biology 17, 734–744.
Sewell, M.A. & Young, C.M. 1999. Temperature limits to fertilization and early development in the tropical sea
urchin Echinometra lucunter. Journal of Experimental Marine Biology and Ecology 236, 291–305.
Shanks, A.L., Grantham, B.A. & Carr, M.H. 2003. Propagule dispersal distance and the size and spacing of
marine reserves. Ecological Applications 13 (Supplement), S159–S169.
Sheppard Brennand, H., Soars, N., Dworjanyn, S.A., Davis, A.R. & Byrne, M. 2010. Impact of ocean warming
and ocean acidication on larval development and calcication in the sea urchin Tripneustes gratilla.
PLoS ONE 5, e11372.
Shirayama, Y. & Thornton, H. 2005. Effect of increased atmospheric CO2 on shallow water marine benthos.
Journal of Geophysical Research 110, C09S08.
Smale, D.A. & Barnes, D.K.A. 2008. Likely responses of the Antarctic benthos to climate-related changes
in physical disturbance during the 21st century, based primarily on evidence from the West Antarctic
Peninsula region. Ecography Pattern and Diversity in Ecology 31, 289–305.
Soars, N., Prowse, T.A.A. & Byrne, M. 2009. Overview of phenotypic plasticity in echinoid larvae, ‘Echinopluteus
transversus’ type vs. typical echinoplutei. Marine Ecology Progress Series 383, 113–125.
Sokolova, I.M. & Pörtner, H.O. 2001. Temperature effects on key metabolic enzymes in Littorina saxatilis and
L. obtusata from different latitudes. Marine Biology 139, 113–126.
Somero, G.N. 2002. Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs
of living. Integrative and Comparative Biology 42, 780–789.
Somero, G.N. 2010. The physiology of climate change: how potentials for acclimatization and genetic adapta-
tion will determine ‘winners’ and ‘losers’. Journal of Experimental Biology 213, 912–920.
Southward, A.J., Hawkins, S.J. & Burrows, M.T. 1995. Seventy years’ observations of changes in distribution
and abundance of zooplankton and intertidal organisms in the western English Channel in relation to ris-
ing sea temperature. Journal of Thermal Biology 20, 127–155.
Stachowicz, J.J., Terwin, J.R., Whitlatch, R.B. & Osman, R.W. 2002. Linking climate change and biologi-
cal invasions: ocean warming facilitates nonindigenous species invasions. Proceedings of the National
Academy of Sciences of the United States of America 99, 15497–15500.
Stanwell-Smith, D. & Peck, L.S. 1998. Temperature and embryonic development in relation to spawning and
eld occurrence of larvae of three Antarctic echinoderms. Biological Bulletin (Woods Hole) 194, 44–52.
IMPACT OF OCEAN WARMING AND OCEAN ACIDIFICATION
41
Staver, J.M. & Strathmann, R.R. 2002. Evolution of fast development of planktonic embryos to early swim-
ming. Biological Bulletin (Woods Hole) 203, 58–69.
Stillman, J.H. 2003. Acclimation capacity underlies susceptibility to climate change. Science 301, 65 only.
Styan, C.A. 1998. Polyspermy, egg size, and the fertilization kinetics of free-spawning marine invertebrates.
American Naturalist 152, 290–297.
Styan, C.A., Byrne, M. & Franke, E. 2005. Evolution of egg size and fertilisation efciency in sea stars: large
eggs are not fertilized more readily than small eggs in the genus Patiriella (Echinodermata: Asteroidea).
Marine Biology 147, 235–242.
Sultan, S.E. 2007. Development in context: the timely emergence of eco-devo. Trends in Ecology and Evolution
22, 575–582.
Suwa, R., Nakamura, M., Morita, M., Shimada, K., Iguchi, A., Sakai, K. & Suzuki, A. 2010. Effects of acidied
seawater on early life stages of scleractinian corals (genus Acropora). Fisheries Science 76, 93–99.
Talmage, S.C. & Gobler, C.J. 2009. The effects of elevated carbon dioxide concentrations on the metamorpho-
sis, size, and survival of larval hard clams (Mercenaria mercenaria), bay scallops (Argopecten irradians),
and Eastern oysters (Crassostrea virginica). Journal of Limnology and Oceanography 54, 2072–2080.
Tewksbury, J.J., Huey, R.B. & Deutsch, C.A. 2008. Putting the heat on tropical animals. Science 320,
1296–1297.
Thatje, S., Anger, K., Calcagno, J.A., Lovrich, G.A., Pörtner, H.-O. & Arntz, W.E. 2005. Challenging the cold:
crabs reconquer the Antarctic. Ecology 86, 619–625.
Thompson, R.C., Crowe, T.P. & Hawkins, S.J. 2002. Rocky intertidal communities: past environmental changes,
present status and predictions for the next 25 years. Environmental Conservation 29, 168–191.
Thorson, G. 1950. Reproduction and larval ecology of marine bottom invertebrates. Biological Reviews
Cambridge Philosophical Society 25, 1–45.
Todgham, A.E. & Hofmann, G.E. 2009. Transcriptomic response of sea urchin larvae Strongylocentrotus pur-
puratus to CO2-driven seawater acidication. Journal of Experimental Biology 212, 2579–2594.
Tomanek, L. 2010. Variation in the heat-shock responses and its implications for predicting the effect of
global climate change on species’ biogeographical distribution ranges and metabolic costs. Journal of
Experimental Biology. 213, 971–979.
Tomanek, L. & Somero, G.N. 1999. Evolutionary and acclimation-induced variation in the heat-shock responses
of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of
thermotolerance and biogeography. Journal of Experimental Biology. 202, 2925–2936.
Travers, M-A., Basuyaux, O., LeGoïc, H., Huchette, S., Nicolass, J-L., Koken, M. & Paillard, C. 2009. Inuence
of temperature and spawning effort on Haliotis tuberculata mortalities caused by Vibrio harveyi: an
example of emerging vibriosis linked to global warming. Global Change Biology 15, 1365–1376.
Truchot, J.P. & Duhamel-Jouve, A. 1980. Oxygen and carbon dioxide in the marine intertidal environment:
diurnal and tidal changes in rockpools. Respiration Physiology 39, 241–254.
Tunnicliffe, V., Davies, K.T.A., Buttereld, D.A., Embley, R.W., Rose, J.M. & Chadwick, W.W. 2009. Survival
of mussels in extremely acidic waters on a submarine volcano Nature Geoscience 2, 344–348.
Turley, C.M., Roberts, J.M. & Guinotte J.M. 2007. Corals in deep-water: will the unseen hand of ocean acidi-
cation destroy cold-water exosystems? Coral Reefs 26, 445–448.
Uthicke, S., Schaffelke, B. & Byrne, M. 2009. A boom-bust phylum? Ecological and evolutionary conse-
quences of density variations in echinoderms. Ecological Monographs 79, 3–24.
Valentine, J.W. & Jablonski, D. 1986. Mass extinctions: sensitivity of marine larval types. Proceedings of the
National Academy of Sciences of the United States of America 83, 6912–6914.
Vernberg, F.J. 1962. Comparative physiology: latitudinal effects of physiological properties of animal popula-
tions. Annual Review of Physiology 24, 517–546.
Veron, J.E.N. 2009. Mass extinctions and ocean acidication: biological constraints on geological dilemmas.
Coral Reefs 27, 459–472.
Visser, M.E. 2008. Keeping up with a warming world; assessing the rate of adaptation to climate change.
Proceedings of the Royal Society Series B 275, 649–659.
Voolstra, C.R., Schnetzer, J., Peshkin, L., Randall, C.J., Szmant, A.M. & Medina, M. 2009. Effects of temperature
on gene expression in embryos of the coral Montastraea faveolata. BMC Genomics 10, 627 (9 pages).
Ward, G.E., Brokaw, C.J., Garber, D.L. & Vacquier, V.D. 1985. Chemotaxis of Arbacia punctulata spermatozoa
to resact, a peptide from the egg jelly layer. Journal of Cell Biology 101, 2324–2329.
MARIA BYRNE
42
Watson, S.-A., Southgate, P.C., Tyler, P.A. & Peck, L. 2009. Early larval development of the Sydney rock
oyster Saccostrea glomerata under near-future predictions of CO2 driven ocean acidication. Journal of
Shellsh Research 28, 431–437.
Wethey, D.S. & Woodin, S.A. 2008. Ecological hindcasting of biogeographic responses to climate change in
the European intertidal zone. Hydrobiologia 606, 139–151.
Whalan, S., Ettinger-Epstein, P. & de Nys, R. 2008. The effect of temperature on larval pre-settlement duration
and metamorphosis for the sponge, Rhopaloeides odorabile. Coral Reefs 27, 783–786.
Widdicombe, S. & Spicer, J.I. 2008. Predicting the impact of ocean acidication on benthic biodiversity: what
can animal physiology tell us? Journal of Experimental Marine Biology and Ecology 366, 187–197.
Wong, E., Davis, A.R. & Byrne, M. 2010. Reproduction and early development in Haliotis coccoradiata
(Vetigastropoda: Haliotidae). Invertebrate Reproduction and Development 54, 77–87.
Wood, H.L., Spicer, J.I., Lowe, D.M. & Widdicombe, S. 2010. Interaction of ocean acidication and tempera-
ture,; the high cost of survival in the brittlestar Ophiura ophiura. Marine Biology 157, 2001–20132.
Wood, H.L., Spicer, J.I. & Widdicombe, S. 2008. Ocean acidication may increase calcication rates, but at a
cost. Proceedings of the Royal Society B 275, 1767–1773.
Wootten, J.T., Pster, C.A. & Forester, J.D. 2008. Dynamic patterns and ecological impacts of declining ocean
pH in a high-resolution multi-year dataset. Proceedings of the National Academy of Sciences of the
United States of America 105, 18848–18853.
Wright, D.A., Kennedy, V.S., Roosenburg, W.H., Castagna, M. & Mihursky, J.A. 1983. Temperature tolerance
of embryos and larvae of ve bivalve species under simulated power plant entrainment conditions: A
synthesis. Marine Biology 77, 271–278.
Yamada, K. & Mihashi, K. 1998. Temperature-independent period immediately after fertilization in sea urchin
eggs. Biological Bulletin (Woods Hole) 195, 107–111.
Young, C.M., Ekaratne, S.N.K. & Cameron, J.L. 1998. Thermal tolerances of embryos and planktotrophic
larvae of Archaeopneustes hystrix (A. Agassiz) (Spatangoidea) and Stylocidaris lineata (Mortensen)
(Cidaroidea), bathyal echinoids from the Bahamian Slope. Journal of Experimental Marine Biology and
Ecology 223, 65–76.
Zeebe, R.E., Zachos, J.C., Caldeira, K. & Tyrrell, T. 2008. Carbon emissions and acidication. Science 321,
51–52.
Zippay, M.L. & Hofmann, G.E. 2010a. Physiological tolerances across latitudes: thermal sensitivity on larval
marine snails (Nucella spp.). Marine Biology 157, 707–714.
Zippay, M.L. & Hofmann, G.E. 2010b. Effect of pH on gene expression and thermal tolerance of early life his-
tory stages of red abalone (Haliotis rufescens) on larval marine snails (Nucella spp.). Journal of Shellsh
Research 29, 429–439.
... 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. ...
Thesis
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. ...
Article
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. ...
Article
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. ...
Article
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. ...
Article
Full-text available
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