Dr Anthony Richardson’s work is recognised internationally for significant contributions in the fields of climate impacts on marine species, plankton dynamics, and linkages between the environment, plankton and fisheries. He has diverse research interests in marine ecology, focusing on understanding the effects of environmental variability on marine systems as a window to predicting impacts of climate change. Research by Dr Richardson and collaborators has provided our first evidence of earlier timing of phytoplankton productivity in the ocean with global warming including the potential mismatch between successive trophic levels. We have also found ocean-basin changes in primary and secondary productivity (increasing near Poles, decreasing near Tropics) over the last 50 years in response to climate change. This knowledge has helped synthesise our understanding of impacts of climate change on pelagic marine ecosystems, has provided seminal knowledge contributing to IPCC Working Group II on Impacts, Adaptation and Vulnerability (IPCC 2007).

Climate Adaptation Flagship, CSIRO Marine & Atmospheric Research. PO Box 120, Cleveland QLD 4163, Australia. .(JavaScript must be enabled to view this email address)

Dr. David McKinnon has over 25 years experience as a biological oceanographer, and has research interests in zooplankton dynamics, planktonic food chains and the microbial loop.  As a principal research scientist within the Australian Institute of Marine Science Water Quality and Ecosystem Health team he leads research into the environmental impacts of tropical aquaculture and on the biological oceanography of Australia’s tropical seas.

Australian Institute of Marine Science. PMB No. 3, Townsville MC, QLD 4810, Australia.  .(JavaScript must be enabled to view this email address)

Kerrie Swadling is a zooplankton ecologist at the University of Tasmania/ Tasmanian Aquaculture and Fisheries Institute who has worked in temperate and polar systems for more than 15 years. Her research interests include the trophodynamics and life history strategies of zooplankton, their role in heavy metal cycling, and the affects of environmental change on zooplankton distribution in the Southern Ocean. Along with her-coauthors, Kerrie was recently awarded a Whitley award for best CD-Rom and Electronic Guide for the ‘Guide to the Marine Zooplankton of southeastern Australia’.

Tasmanian Aquaculture and Fisheries Institute. Private Bag 49, Taroona. Hobart TAS 7053, Australia.  .(JavaScript must be enabled to view this email address)

• short-lived (~1 year) and thus their population dynamics are tightly coupled to climate
• poikilothermic, so their physiological processes are highly sensitive to temperature
• generally not commercially exploited (except krill, a few jellyfish and some temporary members of the plankton known as meroplankton), so long-term trends in response to environmental change are less confounded with exploitation
• sampled over ocean basin scales using plankton recorders.

There are no observed impacts of climate change on zooplankton in Australia, (here we focus on the Australian region within the Exclusive Economic Zone, excluding Australian waters further afield in the Southern Ocean). As extensive impacts have been documented from many other systems around the world, this lack of knowledge in Australia may be due to the lack of data rather than the absence of impacts. Poloczanska et al. (2007), p. 452-453, state that “Globally there are zooplankton time series spanning more than 15 yr in no fewer than 30 countries, including relatively small or developing nations such as Bulgaria, Chile, Estonia, Greece, Kazakhstan, Latvia, Faroe Islands, Namibia, Peru, Turkey and the Ukraine. However, the longest ongoing zooplankton time series in Australia is 2 yr and consists of a single cross-shelf transect off Perth. Given the diversity of marine habitats in Australia and the economic and social importance of fishing, Australia is clearly impoverished in long-term zooplankton and other datasets are urgently required to assess climate change impacts …”

The time series off Perth referred to in this passage is no longer operational and ended after 2 years. In the following sections, we necessarily draw on knowledge of impacts of climate change on zooplankton from research around the world to address what we perceive as the three most important climate change drivers of zooplankton: temperature, acidification and nutrient enrichment.

Temperature
Impacts of warming on zooplankton manifest as poleward movements in the distribution of individual species and of assemblages, earlier timing of important life cycle events (phenology), and changes in abundance and community structure. Each is discussed below.

Distribution
Many zooplankton species to expand their ranges poleward as temperatures warm (as is the case for other animals). The most striking examples are from the Northeast Atlantic, where members of the warm-water copepod assemblages have moved more than 1,100 km polewards (north) over the past 50 years (Beaugrand et al. 2002). For example, the calanoid copepods Centropages chierchiae and Temora stylifera have both moved north from off the Iberian Peninsula in the 1970s and 1980s to the English Channel in the 1990s (Lindley and Daykin 2005). Concurrent with this poleward expansion of warm-water copepods, Arctic copepods have retracted to higher latitudes (Beaugrand et al. 2002).

These shifts in distribution have had dramatic impacts on the foodweb of the North Sea (Beaugrand et al. 2003). In particular, the cool-water copepod assemblage, which has high biomass and is dominated by relatively large species that peak in abundance in spring, has retracted north (polewards) as waters have warmed. It has been replaced in the North Sea by the warm-water assemblage, which typically has lower biomass and contains smaller species that peak in abundance in autumn and not spring. This is critical because Atlantic cod Gadus morhua, traditionally a major fishery of the North Sea, spawn in spring, and at this time cod larvae require a diet of large copepods. If this food source is not available, larval mortality is high and recruitment to the fished stock is poor. Since the late 1980s, when the cool-water assemblage was replaced by the warm-water one, there has been very low copepod biomass during spring in the North Sea, and cod recruitment has plummeted (Beaugrand et al. 2003).

The range shifts exhibited by zooplankton in response to global warming, with a mean translocation of ~200 km per decade (Richardson 2008), are among the fastest and largest of any group, marine or terrestrial. By comparison, a global meta-analysis of range shifts across 99 species of birds, butterflies, and alpine herbs found that they moved polewards (or upwards) by an average of only 6.1 km per decade (Parmesan and Yohe 2003). If the range shifts highlighted here for zooplankton are anywhere near typical of those experienced more broadly in the plankton, they would dwarf those reported from terrestrial systems. Such substantial range changes mean that there will be considerable spatial re-organisation of existing zooplankton communities, and this would be expected to occur in Australia also.

Finally, there is some unpublished anecdotal evidence that some subtropical copepod species are extending their range polewards along the coast of Tasmania as a result of the southward penetration of the East Australian Current, but this is yet to be confirmed.

Phenology
Phenology is the timing of important biological events. Substantial phenological changes in plankton communities have been observed in temperate regions of the North Atlantic and North Pacific. As a group, the meroplankton, which includes larvae of bryozoans, bivalves, barnacles, crabs, seastars and fish, are particularly sensitive to climate change. In the North Sea, for instance, the meroplankton assemblage has advanced their appearance in the plankton by 27 days over the past 45 years, although some groups have reacted more strongly than others. For example, larvae of benthic echinoderms are now appearing 47 days earlier than they did 50 years ago, when waters were on average 1°C cooler (Edwards and Richardson 2004). This earlier appearance is probably a consequence of warmer temperatures stimulating physiological development and larval release (Kirby et al. 2007). Similarly, observations off Helgoland (Germany) in the southern North Sea for 1990–1999 reveal that fish larvae are also sensitive to changes in water temperature, with more than one-third of the species studied exhibiting significant correlations between the middle of their seasonal peak in abundance and mean temperature (Greve et al. 2005).

Intriguingly, the timing of the abundance peak of various plankton functional groups seems not to respond to ocean warming synchronously, resulting in predator–prey mismatches that could resonate to higher trophic levels (Edwards and Richardson 2004). Over the past 45 years, dinoflagellates in the North Sea are peaking earlier by 23 days, diatoms by 22 days, but copepods and other holozooplankton (e.g. amphipods, chaetognaths) by only 10 days. This differential response of phytoplankton and zooplankton may lead to a mismatch between successive trophic levels and a change in the synchrony between primary, secondary, and tertiary production. Efficient transfer of marine primary and secondary production to higher trophic levels, such as those occupied by commercial fish species, depends largely on the temporal synchrony between successive production peaks, especially in temperate marine systems (Cushing 1990). Such synchrony, necessary for successful fish recruitment, could be disturbed by climate change.

The most striking example of observed ecosystem repercussions of climate-driven changes in phenology is evident in the Subarctic North Pacific Ocean (Mackas et al. 1998). Here a single copepod species, Neocalanus plumchrus, dominates the zooplankton biomass. The timing of its annual maximum has shifted dramatically over the past 50 years, with peak biomass 60 days earlier in warm than in cold years. The change in developmental timing is probably a consequence of both increased survivorship of early cohorts in warm years and physiological acceleration. The timing of the zooplankton biomass peak is ecologically significant because it influences the availability of food to upper-ocean predators such as salmon, herring, hake, and seabirds. For example, the world’s largest colony of the planktivorous seabird, Cassin’s auklet Ptychoramphus aleuticus, occurs in British Columbia and the birds prey heavily on Neocalanus during the breeding season (Bertram et al. 2001). When conditions are warm, spring is early, and the duration of overlap of seabird breeding and Neocalanus availability in surface waters is very short resulting in a limited period of food availability to feed chicks. In these circumstances, a mismatch between prey and predator populations arises, resulting in starvation and reduced growth of chicks. During cold years, spring is later and there is tighter synchrony between food availability and the timing of breeding. In this way, the reproductive performance of Cassin’s auklet is compromised in warmer years relative to that in colder years. If this species does not adapt to the changing food conditions, global warming could diminish its long-term survival chances.

Several generalisations emerge from phenological studies of zooplankton. The first is that observed changes in zooplankton appear significantly greater than those observed for taxonomic groups on land. In a phenological study of 172 species of herbs, shrubs, trees, birds, butterflies, and amphibians, Parmesan and Yohe (2003) noted a mean phenological change of 2.3 days per decade. Root et al. (2003) calculated the phenological shift for invertebrates, amphibians, birds and trees, and found mean phenological changes of 3–6 days. By contrast, the mean phenological change observed for zooplankton is significantly greater at 7.6 days per decade (Figure 2). Second, the phenology of phytoplankton appears to be more sensitive than zooplankton, consistent with terrestrial plants and grazers. Undoubtedly, over historical time, these predator–prey systems have undergone substantial temperature changes and remained viable, so it is critical to establish how long it will take for these phenological relationships to adapt to the warmer temperatures and resynchronize, especially with other concomitant anthropogenic stressors. Such predator-prey mismatch could be happening in temperate Australian waters, but we have no data to assess it. Last, responses to global warming are species-specific and may be determined by the coincidence of warming with critical life cycle stages or events. This suggests that an intimate knowledge of the life history of an organism may be needed for an adequate explanation of population impacts and prediction of ecosystem responses.

Figure 2. Changes in phenology from different studies (mean ± s.e.). Reproduced from Richardson (2008). Data for groups other than zooplankton from Root et al. (2003).

Abundance
Changes in abundance are more difficult to attribute to global warming than are shifts in distribution or phenology, although they may have greater ecosystem ramifications (Richardson 2008). Although most evidence of climate impacts on zooplankton is from the northern hemisphere because this is where most zooplankton research is concentrated, there have been dramatic changes documented elsewhere. Since the 1970s, there has been a decline in krill (Euphausia superba) biomass in the Southern Ocean and a concomitant increase in salps, which occupy less productive and warmer regions (Atkinson et al. 2004). It is likely that these changes are a consequence of global warming. Strong summer phytoplankton blooms and winters of extensive sea ice, with plentiful food from ice algae, enhance survival of krill larvae and their recruitment to adult stocks. As waters have warmed, the extent of winter sea ice and its duration have declined, which is likely to have impaired larval krill survival and led to the decline in krill density. Warmer waters also provide more favourable habitat for salps. Declining krill populations could be deleterious to the populations of baleen whales, fish, penguins, seabirds and seals that depend on krill as their primary food source.

One of the most striking examples of changes in abundance in response to long-term warming is from foraminifera in the California Current (Field et al. 2006). Throughout the 20th century, the number of tropical/subtropical species has been increasing, reflecting a warming trend; this phenomenon is most dramatic after the 1960s. This change towards tropical foraminifera echoes similar increases in abundance of many other subtropical and tropical animals and decreases in temperate algae, zooplankton, fish, and seabirds in the California Current over the past few decades.

Ocean acidification
This section is not meant to be exhaustive as there is a separate section (by Howard et al.) on effects of acidification, but this issue is important enough to discuss it briefly here. Calcium carbonate structures are present in a variety of important zooplankton groups including molluscs (e.g., snails), echinoderms (e.g., seastars, sea urchins), foraminifera and some crustaceans (Raven et al. 2005). The direct effect of ocean acidification on calcifying zooplankton will be to partially dissolve their shells, increasing shell maintenance costs and reducing growth. But even among marine organisms with calcium carbonate shells, susceptibility to acidification varies depending on whether the crystalline form of their calcium carbonate is aragonite or calcite. Aragonite is more soluble under acidic conditions than calcite, making it more susceptible to dissolution. As oceans continue to absorb CO2, undersaturation of aragonite and calcite in seawater will be initially most acute in the Southern Ocean and then move northward. There will also be synergistic impacts between effects of acidification and warming on organisms.

Winged snails known as pteropods are likely to be the zooplankton group most vulnerable to ocean acidification because of their aragonite shells. In the Southern Ocean, pteropods are prominent components of the food web, contributing to the diet of carnivorous zooplankton, many fish species and baleen whales, as well as forming the entire diet of another group of pelagic snails, the gymnosomes. Pteropods in the Southern Ocean also account for the majority of the annual flux of both carbonate and organic carbon exported to ocean depths. Because these animals are extremely delicate and difficult to keep alive experimentally, precise pH thresholds where deleterious effects commence are not known. However, even experiments over as little as 48 hours show shell deterioration in the pteropod Clio pyrimidata at atmospheric CO2 levels approximating those likely around 2100 under a business-as-usual emissions scenario (Orr et al. 2005). If pteropods cannot grow and maintain their protective shell, their populations are likely to decline and their range will contract towards lower-latitude surface waters (equatorwards) that remain supersaturated in aragonite provided, they can adapt to the warmer temperatures there. This would have obvious repercussions throughout the food web of the Southern Ocean.

In tropical Australian waters of the Great Barrier reef, pteropods such as Creseis spp. and Cavolinia longirostris (Figure 3) are important members of the zooplankton community (McKinnon et al. 2007), and are particularly abundant in December and January respectively. Within the next 100 years, first the aragonite and then the calcite saturation state of Australian waters could decline below levels needed for shell formation and maintenance in calcifying plankton organisms. Under-saturation of aragonite and calcite in sea water is likely to be more acute at higher latitudes and then move toward the equator. Pteropods are likely to decline and may eventually disappear in response to ocean acidification.

Figure 3. The pteropod Cavolinia longirostris is threatened by acidification of Great Barrier Reef waters. Image courtesy of Russ Hopcroft, University of Alaska, Fairbanks (c) 2007.

Another group potentially sensitive to ocean acidification is the Foraminifera; after death their tests contribute a significant proportion of the sediments in many sandy regions in tropical Australia, Although they are formed from calcite and are thus less susceptible to ocean acidification than organisms composed of aragonite, calcite-producing foraminifera are likely to be negatively impacted by reduced pH in the longer term.
Finally, a recent study in the North Sea suggested that jellyfish increase in abundance as pH declines; this was interpreted as the negative impact of more acidic conditions on calcifying plankton opening up ecological space for jellyfish (Attrill et al. 2007). However, a more comprehensive analysis over a larger area showed no significant relationship between jellyfish abundance and acidity (Richardson and Gibbons 2008). Instead, more acidic conditions could potentially negatively affect jellyfish, given that most scyphozoan and some hydrozoan medusae use calcium carbonate statoliths for orientation. Whether statoliths are negatively affected by reduced pH, as is likely for other calcium carbonate structures of marine plankton (e.g. pteropod shells), or whether they are sufficiently protected within the jellyfish, is currently unknown.

Nutrient enrichment
In many regions of the world, indirect impacts of climate change on nutrient enrichment could outweigh direct impacts of temperature change and acidification. In particular, oligotrophic (low nutrient) tropical regions with little seasonality, such as those in Northern Australia, could be very sensitive to changes in nutrient enrichment.
Physical atmospheric and oceanic processes drive nutrient enrichment, and thus phytoplankton and zooplankton abundance, size structure, and community composition (Figure 4). Most productivity in the oceans is by phytoplankton in the sun-lit upper layer (top 100 m). In coastal regions, nutrients are delivered to plankton communities through river run-off and wind-borne dust, and through oceanic enrichment processes such as wind-driven coastal upwelling. Further offshore, oceanic divergences such as fronts, eddies and turbulent wind-mixing can increase nutrient concentrations in the surface zone.

Figure 4. Schematic highlighting the role of nutrient enrichment, determined by physical processes, in regulating plankton ecosystem structure. Changes to the physical processes that lead to nutrient enrichment lead to plankton communities dominated by large phytoplankton (diatoms) and crustacean zooplankton, and physical processes that lead to lower nutrient conditions lead to ecosystems dominated by very small phyto- and zooplankton. From Fig. 6.3 in McKinnon et al. (2007).

Changes to these physical processes as a consequence of climate change will alter nutrient enrichment and plankton communities, with lower nutrient conditions leading to less plankton, and enhanced nutrient conditions resulting in greater plankton abundance. Phytoplankton and zooplankton community structure will also change, with picoplankton and the nitrogen-fixing cyanobacterium Trichodesmium (in tropical regions) likely to be more important if nutrient input processes decline (Figure 1). As a result, under low nutrient conditions, small non-crustacean zooplankton and gelatinous filter-feeding groups (pelagic tunicates such as salps, doliolids, appendicularia) are more prominent, while enhanced nutrient conditions favour larger crustacean zooplankton. Under nutrient rich conditions, diatoms increase, leading to more crustacean zooplankton and carnivorous medusae and ctenophores.
An illustration from the Northeast Atlantic highlights the effect that global warming can have on stratification and zooplankton abundances (presumed to operate through changes in nutrient enrichment), and emphasizes the region-specific consequences (Richardson and Schoeman 2004). In this region, phytoplankton become more abundant with warming of cool, windy, and well-mixed regions, probably because warmer temperatures boost metabolic rates and enhance stratification, thereby increasing the amount of time phytoplankton cells spend in the euphotic zone. However, phytoplankton become less abundant when already warm regions get even hotter, probably because warmer surface water blocks further nutrient-rich deep water from rising to the euphotic layer. This regional phytoplankton response is transmitted up the plankton foodweb to herbivorous copepods and carnivorous zooplankton.

Warming is likely to expand the distribution of many southern hemisphere zooplankton species polewards, as has been the case in the Northern Hemisphere. As the general warming trend in eastern Australia has been exacerbated by a strengthening of the warm southward-flowing East Australian Current over the past 60 years (Ridgway 2007), more striking changes are expected on the east than the west coast of Australia. Responses of species to climate change will vary, with some species responding faster then others and some not responding at all. This will lead to a re-organisation of plankton communities.

Warming could expand the distribution of many of the most venomous tropical jellyfish species toward subtropical and temperate latitudes (Richardson et al. 2009). For example, the northeast Australian coast is home to two types of box jellyfish: the sea wasp Chironex and the species complex known as irukandji; stings from both can be fatal to swimmers and force beach closures. With warming, there is the potential for box jellyfish to move southward toward more populated areas, which would have severe repercussions for the tourist industry.

Global warming could lead to increases in abundance of some other jellyfish species. In an analysis of 15 long-term jellyfish and ctenophore time-series, Purcell (2005) found that 11 species increased in abundance with warming. She concluded that temperate species may benefit from global warming, but tropical jellyfish could decline in abundance because many species may have a thermal maximum around 34–35°C. Further, experimental evidence suggests that jellyfish exhibit faster rates of both asexual and sexual reproduction at warmer temperatures (Purcell 2005).

Calcifying organisms with aragonite shells, such as the pteropods in the Southern Ocean, are likely to be negatively affected by the 2030s. Tropical pteropods in Northern Australia, such as Creseis spp. and Cavolinia longirostris, may decline in abundance. Survival of mussel and echinoderm (e.g., seastars, sea urchins) larvae are also likely to be affected by 2100. Calcifying species in southern Australian waters could find themselves caught in a squeeze between the need to move southwards as waters warm and the need to move northwards as low pH waters expand northwards in the Southern Ocean.

In temperate and polar regions, marked changes in phenology will happen as waters warm. As not all species will respond similarly, there is likely to be trophic mismatch, between grazers and their phytoplankton food, and between predators and their prey. Because the amount of phytoplankton and zooplankton in a region is likely to influence the carrying capacity of fish (Ware and Thompson, 2005), such trophic mismatches could result in reduced energy flow to higher trophic levels and ultimately lower fish yield in some regions.

Nutrient enrichment could be key to determining the abundance and size of the zooplankton community, through its regulation of phytoplankton abundance and size structure. Although future productivity around Australia is highly uncertain, one recent model suggests that primary and secondary production will increase around most of Australia (Brown et al. in 2009). This could lead to higher fisheries yields.

Altered phytoplankton and zooplankton abundance, composition, productivity and timing of occurrence will have a cascading effect on higher trophic levels. Any decline (or increase) in overall abundance, growth and trophic efficiency of phytoplankton and zooplankton communities is likely to lead to the decline (or increase) in higher trophic levels. Larvae of almost all fishes feed on copepod nauplii at first feeding, and therefore variations in the timing and extent of copepod reproduction could influence patterns of recruitment of fishes and economically important invertebrates, especially those with a long larval life, such as crayfish.

• There are no observed impacts of climate change on zooplankton in Australia; this is probably due to the lack of long-term datasets on zooplankton

• Based on knowledge of impacts of climate change on zooplankton from research around the world, the three most important aspects of climate change for zooplankton are temperature, acidification and nutrient enrichment

• Globally, zooplankton distributions are moving poleward as seas warm, leading to new re-arrangement of plankton communities

• Anecdotally, there is evidence that some subtropical species are extending their range polewards along the coast of Tasmania as a result of the southwards (polewards) penetration of the East Australian Current, while typically cold water species are retracting further south

• The phenology (timing) of zooplankton peak abundance in the northern hemisphere appears to be responding faster than that of terrestrial animals and plants, and we do not know whether this is happening in the southern hemisphere also

• In temperate and polar regions, the timing of peaks in abundance of various plankton functional groups does not always respond to ocean warming synchronously, resulting in predator–prey mismatches

• Indirect impacts of climate change on the nutrient enrichment regime could outweigh the direct impacts of temperature change and acidification, particularly in oligotrophic (low nutrient) tropical regions with little seasonality, such as those in northern Australia

• Nutrient enrichment changes in Australia are likely to be critical in determining future fisheries yield

• In Australia, we are likely to start losing calcifying zooplankton such as pteropods first from the south of Australia and later from further north

• Changes to the zooplankton community in response to changes in temperature, acidification and nutrient enrichment will resonate throughout Australian marine ecosystems

Distribution, Phenology, Abundance/community structure, Acidification, Nutrient enrichment
There is LOW evidence and LOW confidence. This is because there is no evidence yet in Australia due to a lack of long-term time series.

Distribution
There is HIGH evidence from observed impacts elsewhere and HIGH consensus in those findings.

Phenology
There is MEDIUM evidence from observed impacts elsewhere and MEDIUM consensus in those findings.

Abundance/community structure
There is LOW evidence from observed impacts elsewhere and LOW consensus in the type of response

Acidification
There is MEDIUM evidence from laboratory work and MEDIUM consensus in those findings.

Nutrient enrichment
There is LOW evidence from observed impacts elsewhere and models, and LOW consensus in the type of response