Leading up to Halloween night, I recently embarked on a #scicomm project via social media (Facebook and Twitter), sharing information about #SevenSpookySpecies from the ocean. The project was fairly successful in engaging people on Facebook (95 likes, 19 interactive comments, and 3 shared posts), and Twitter (26 likes and 23 retweets). I was able to spark interest in followers by introducing people to the the biology of skeleton shrimps, vampire squids from hell, ghostly shrimps, humpbacked anglerfish, creepy crawly spider crabs, giant isopods, and alien amphipods. I very much enjoyed delivering this series of fun (and maybe a little bit creepy) marine species. In fact, I plan to make this an annual series leading up to Halloween. Nonetheless, I wanted to make it accessible for those who may have missed my posts.
So without further ado, here are my picks for this year’s #SevenSpookySpecies!
#7. Skeleton shrimp, Caprella mutica
Commonly known as the Japanese skeleton shrimp, Caprella mutica is native to eastern Asia and is considered an invasive species in Atlantic Canada, first reported in the Bay of Fundy in the 1990s (although it’s ecological impacts as an invader are not well understood). These guys can often be found in high densities on ropes, buoys, mussel socks, and other man-made structures. They are quite small, with males reaching a maximum size ~3.5 cm and females reaching a maximum size ~1.5 cm. The males’ neck and claws are super hairy and the males also have a segmented neck (2 segments).
#6. Ghost shrimp, Neotrypaea californiensis
Ghost shrimps (Neotrypaea californiensis) are an intertidal species found on the Pacific coast of North America. These shrimps are fairly pale in appearance and can reach a maximum size of just under 12 cm body length. Neotrypaea californiensis live underneath the sediment surface in U-shaped burrows that reach to the surface of the sediment – as such, they’re referred to as “infaunal” species (species living within the sediment). These burrows have many branches or arms and support a diverse array of other species, including snapping shrimps, copepods, crabs, and clams.
In Canada, they can be found in soft-sediment intertidal habitats (mud- and sandflats) of British Columbia where they residewith other infaunal shrimps (mud shrimps, Upogebia pugettensis). Together with mud shrimps, ghost shrimps can often be found in high densities, which can result in significant amounts of bioturbation (i.e. sediment disturbance). Because they are such efficient bioturbators, it is thought that ghost shrimps (and mud shrimps) positively affect their surrounding ecosystem increasing primary and secondary productivity, and by reducing the system’s susceptibility to eutrophication (nutrient loading). However, this bioturbation can have negative effects on the production of oyster beds and they’re often considered pests. As such, mudflats with high densities of mud and ghost shrimps are often sprayed with insecticides to remove the “pests”. These shrimps are also often used by fishermen as bait.
The adults of this species display claw dimorphism (or claw asymmetry) – meaning that one claw is bigger than the other. This feature is more pronounced in males, where the large claw can account for as much as 25% of the male’s body mass (see image below) – imagine one of your hands occupying 25% of your weight! The larger claw in males is thought to be used when two individuals are competing for a mate and is thus likely an evolutionary product of sexual selection.
#5. Spider crab, Macrocheira kaempferi
Having the largest leg span of any living arthropod, the Japanese Spider Crab (Macrocheira kaempferi) resides in the waters off of Japan. This species can have a leg span of up to 18 feet (5.5 meters) from claw to claw and is thought to live up to 100 years (although ageing crustaceans has proven difficult). M. kaempferi can weigh up to >40 lbs, making it the second heaviest living arthropod, (second to the American Lobster).
Japanese Spider Crabs use their thick and durable exoskeleton to protect themselves from predators. However,they also utilize camouflage to avoid being detected by their predators, as their carapace blends well with the sea bottom. Even more, these crabs use a super cool behaviour called decorating to disguise themselves, whereby they cover their shells in algae, sponges, and other plants and animals to enhance its cryptic appearance on the ocean floor.
Japanese Spider Crabs are omnivorous. They can use their claws to gather seaweed and algae from the ocean floor, or to pry open the shells of shellfish. Additionally, these crabs are also known to scavenge on the carcasses of dead animals on the sea floor. A small fishery for this species exists in Japan. However, population declines have meant that fishermen need to fish deeper waters to catch this species and have initiated considerable conservation efforts to protect their populations. Nonetheless, these crabs aren’t an easy catch, as they are very fast and can cause considerable damage to humans with their strong claws and long reach!
#4. Vampire squid (from Hell), Vampyroteuthis infernalis
Not an octopus, not a squid, and residing in deep temperate and tropical seas, Vampyroteuthis infernalis (which translates to “vampire squid from Hell”) is a small cephalopod reaching a maximum body length of ~30 cm. This animal is unique in that it contains the features of two other groups of cephalopods: octopuses and squids! The vampire squid has 8 arms (like an octopus) which support a web of tissue. Concealed behind this web of tissue are two “retractile sensory filaments” – sensory structures akin to squid tentacles that retract into pockets of tissue that are used to detect predators and prey (and other environmental attributes). As such, the vampire squid is placed in its own Order taxonomically – the Vampyromorphida. Because the Vampyromorphida have the features of both octopuses and squids, it is thought that this group of animals may represent a common ancestor to modern octopuses and squids. Interestingly, Vampyroteuthis infernalis is the only extant (still living) species of Vampyromorphida (as far as we know; we still have a lot to learn about the deep sea).
Behaviourally, when these animals are threatened, they use a defense response known as the “pumpkin” or “pineapple” posture. When a vampire squid is threatened by a predator or superior combatant, it throws its arms back over its body and the web of tissue acts as a “cape”. When the cape covers the body, it displays intimidating (but completely harmless; they’re simply constructed of soft tissue) spines, or “fangs”; hence the vampire reference. In addition, the animal uses bioluminesence when in the “pumpkin” or “pineapple” posture, where the tips of its arms flash light and trick a predator into biting the tips of its arms, rather than biting vital structures. Luckily, if a predator does dismember a vampire squid’s arms, they can regenerate.
A vampire squid from Hell that displays a pumpkin posture – definitely a spooky species!
#3. Humpback anglerfish, Melanocetus johnsonii
Chosen as species #3for its Quasimodo-esque name (of course, any anglerfish would suffice as a spooky species), Melanocetus johnsonii is a species of anglerfish belonging to the family Melanocetidae, which are more commonly known as “the black seadevils”. This species lives in the deep sea and can reach depths of up to 4500 m below the surface. M. jonsonii is considered fairly ubiquitous, having been found in tropical and temperate waters of all five oceans.
As in other anglerfishes, female M. johnsonii (max. size of 18 cm) are much larger than the males (< 3 cm). It is black in colour and has a broad, deep head with
very small eyes. Like other anglers, the humpback anglerfish possesses an illicium (or esca) – a “fishing lure” – on its head. This lure dangles near the angler’s mouth and uses bioluminescence to attract prey (remember Finding Nemo?). These predators can consume fairly large prey items – indeed a 5 cm female is recorded to with 3 fish >10 cm body length in its stomach!
While it is certainly most difficult to study anglerfish behaviour, their reproductive strategies are fairly well known. In many anglerfishes, when a male finds a female mate, he attaches himself to her permanently and acts as a parasite, releasing sperm and mating with the same female for the duration of their existence (i.e., males are often monogamous). However, while male M. johnsonii do attach to females for mating, they do not attach permanently, release from the female once she has been inseminated, and will seek other mates.
#2. Giant isopod, Bathynomus giganteus
If you’ve ever turned over an old log, you may have noticed a number of small, grey “bugs” that are commonly referred to as woodlice or pill bugs. These actually aren’t insects, but belong to a group of arthropods known as the Isopoda! While the thought of those little woodlice may have your skin crawling, they pale in comparison to their deep-sea relatives, the giant isopods!
Giant isopods belong to the genus Bathynomus, of which there are approximately 18 species. Within this genus, Bathynomus giganteus – first described in 1879 – is often considered the largest isopod in the world with a maximum length of 76 cm and a maximum weight of just under 4 lbs. It is likely, however, that other Bathynomus species likely reach comparable sizes. Given their overwhelming size, giant isopods are a great example of deep sea gigantism (the tendency of deep sea species to be far larger than their shallow-water counterparts).
The morphology of giant isopods is highly similar to their terrestrial relatives (woodlice) except for the obvious difference – their size! B. giganteus are scavengers on the sea floor and can be found at considerable depths of >2,000 meters (but also at shallower depths of approximately 170 m)! As such, B. giganteus must be able to withstand incredible pressure and extremely low temperatures (which is one potential explanation for deep sea gigantism).
These isopods are primarily carnivorous scavengers, feeding on pelagic animals that perish and sink to the sea floor. They may also act as predators, eating live animals on the sea bottom. Because food is scarce in the deep sea (another potential explanation for deep sea gigantism), however, giant isopods will essentially eat whatever they come across. When they do find food, they often gorge themselves to the point that they can no longer move (kind of like after a big Thanksgiving turkey). They are also thought to be fairly aggressive animals, as they’ve been documented attacking trawl cages and live fish – one was once filmed attacking a shark by latching onto and eating the shark’s face! While that might sound a bit unnerving, you might consider doing the same thing if you had to go upwards of 5 years without eating (as I said, food is scarce in the deep sea)!
#1. Alien amphipod, Phronima sedentaria
Phronima sedentaria is a deep sea amphipod that can be found at depths of up to1,000 m. The females of this species can reach lengths of >4 cm and are larger than males, which only reach up to 1.5 cm. P. sedentaria resides in temperate, subtropical, and tropical waters and can be found in all five of the world’s oceans. While it can reach extreme depths of up to 1,000 m, it is most commonly found in midwater pelagic habitats and can even be found at the surface.
So you may be wondering why the hell I chose this species as my most favorite spooky species – this little guy doesn’t seem so scary at all! That is until you realize that the queen Xenomorph in “Alien” is likely based on this tiny deep sea amphipod. While much smaller than the alien queen, the outward appearance is highly similar. For a super detailed comparison between the two, check out this killer post from Michael Bok at Southern Friend Science published back in 2010.
Not only do these amphipods look like Xenomorphs, but P. sedentaria also exploits a host organism to reproduce – just like Xenomorphs! Females will hunt for salps, consume all of their living tissue to hollow them out, and essentially live inside the hollowed-out salp “barrel”. The female amphipods then use their specialized appendages (known as pleopods) to propel the barrel through the water in search of more prey, and can even do somersaults to quickly change direction. So they essentially kill, eat, and hollow out these salps, and use them as a vehicle to cruise around the deep sea in. Then, when they’re ready, the females will lay their eggs inside the barrel, where the eggs will develop and eventually hatch. Once the larval amphipods hatch, they use the salp barrel as food. When they inevitably grow up into adult amphipods, P. sedentaria become carnivorous predators, feeding predominantly on zooplankton, krill, and arrowworms – they can even take down prey more than twice their own size!
This afternoon I engaged in a Twitter conversation with some colleagues regarding the use of the term dreissenid in the context of “dreissenid mussels”. Colleague A wanted to know if dreissenid should be italicized. I assured her that it indeed does not, because Dreissenidae is a family of mussels containing 3 genera and is not a single genus (to which she obliged). Colleague B then questioned this and asked what to do if using the term when only referring to the genus Dreissena, whereby I suggested using a more specific term (i.e., Dreissena spp.). Colleague A then responded that she originally wanted to use the term to describe only the genus Dreissena, and that this was common practice. Then I got annoyed (again) at common names in general…
So which is it – does dreissenid refer to the family Dreissenidae or the genus Dreissena?
The answer is that it’s commonly used for both. Although many scientists may not care about or acknowledge this, the interchangeability of common names across different taxonomic resolutions can be problematic for a number of reasons.
Let’s first look at a relatively simple example. Say I published a paper on “dreissenid mussels” in the Journal of Crappy Nomenclature, and in the introduction made the claim that there are 16 species of dreissenid mussels. Without context, the reader has no idea as to whether there are 16 species within the family Dreissenidae or 16 species within the genus Dreissena unless they search this information themselves (there are 16 species in the family Dreissenidae; Figure 1).
Likewise, let’s say that in the same paper I was to claim that dreissenid mussels reside in supraterranean (above ground) freshwater systems. While that is true for the genus Dreissena, there exists a subterraneous genus of Dreissenidae (Congeria; resides solely in cave river systems). Again, without context, the reader would be left searching such information. Unfortunately, many readers would not recognize the need to search for this information and would likely apply the information obtained from the two statements outlined above in the context of how they interpret the term “dreissenid mussels”, which may be correct or incorrect depending on my definition of “dreissenid mussels”. Thus, in subsequent publications obtaining information from my hypothetical paper on dreissenid mussels, information may be incorrect, but nonetheless become “common knowledge”.
While the above examples may appear extreme, particularly for those who study these mussels, the points still stand – and for many more taxa than the example herein. Researchers conducting work on species new to them must learn as much about their new study species and related taxa as possible. In this way, using common names interchangeably across levels of taxonomic resolution can easily create problems for these researchers and the propagation of incorrect biological information may result. Furthermore, other problems with common names arise when even more generic terminology is used, like “cushion stars”.
Ultimately, there are two ways to solve the problems outlined above: either define the range of taxa (up front) that a common name being used encompasses, or stop using common names all together. If we are to follow the biological writing rules of Dr. Pechenik (i.e., more concise = better), scientific works would benefit from the elimination of common names (for example, “Dreissena spp.” consumes less space than “dreissenid mussels”, and the former would not require a formal definition). Not only does the use of precise taxonomic nomenclature reduce verbiage, but it would remove the potential for misinterpretation with respect to the breadth of biological processes across various levels of taxonomic resolution. That, and we would negate complex Twitter conversations regarding how to use common nomenclature and have more time to spend on writing our actual papers…
So, in conclusion, just stop using common names. They suck.
At some point or another, you’ve probably read or heard the common headline:
“Climate change threatens ____________ (insert your favorite species).”
But once you’ve digested the doom-and-gloom story, have you ever wondered how we know how climate change impacts various marine species? What is it that scientists do that leads to such claims? Are these claims legitimate? How accurate are they?
When assessing the impacts of climate change on living organisms, most studies employ controlled experiments, where researchers can tinker with one or a number of relevant variables to mimic predicted future conditions and observe how organisms respond to these conditions. There are substantial problems with this approach, however. First, biological responses are typically assessed in the context of only one or two environmental stressors, while we know that a multitude of factors (e.g., temperature, acidification, eutrophication, hypoxia, salinity, etc.) will have independent and/or synergistic biological impacts. Second, over the duration of such experiments, conditions are often kept constant, mimicking average future conditions. Finally, studies typically assess species in isolation, which doesn’t adequately address the community and/or ecosystem consequences of climate change, nor how individual species will respond when residing in their natural habitats. Consequently, I argue that the biological effects of a changing climate are, at present, poorly understood.
The ways in which organisms respond to a given environmental stressor do not solely depend on that single stressor. The interactive effects of multiple environmental stressors can elicit drastically different biological responses. For example, it is increasingly recognized that food availability can modulate the magnitude of effect when assessing the biological impacts of climate change in the ocean, suggesting that, at least physiologically, many species can tolerate a warming and acidifying ocean as long as they have enough energy to do so. In a recent literature review of the behavioural impacts of ocean acidification (Clements & Hunt, in review), we found that 7/8 publications incorporating the independent and synergistic effects multiple environmental stressors (Table 1) in experiments derived different conclusions than when acidification was tested in isolation. Furthermore, the outcomes were all over the board, with additional stressors attenuating, amplifying, or not affecting the behavioural endpoint in question. The problem is that only 8/57 studies actually addressed the effects of multiple environmental stressors – a problem that transfers other biological responses to climate change as well.
It doesn’t take a rocket scientist to know that nature is far from stable. Growing up in the Maritime Provinces of Canada, I know that a look out the window from one moment to the next can yield drastically different weather observations. While the term “weather” applies to environmental phenomena over small temporal scales (hours, day, weeks, months, etc.), “climate” refers to the average of those weather conditions over long periods of time (years, decades, centuries, millennia, etc.). Since climate is a function of weather, understanding the impacts of climate change requires incorporating an understanding of the weather that derives the climate. The variability (i.e., the weather) around projected climatic means can modulate the amount of time that an organism experiences environmental conditions above or below a threshold whereby the organism is affected (Figure 1). Unfortunately, few studies take variability into consideration. In the same literature review mentioned above (Clements & Hunt, in review), only 1/57 studies took variability into consideration, reporting a negative effect of acidification + variability, while acidification alone elicited no effect. Furthermore, studies incorporating multiple environmental stressors and their associated variability are virtually non-existent. Ultimately, a strong understanding of how climate change influences biology requires embracing variability, not dismissing it – otherwise our understanding remains flawed.
Species interactions can also elicit different responses to climate change. For example, the presence of marine plants and their density/abundance within a given marine system can, to an extent, buffer oceanic pH and mitigate the impacts of ocean acidification to other organisms residing within that system. As such, understanding the impacts of climate change in terms of community- and ecosystem-wide consequences not only provides a broader understanding of the biological and ecological impacts of climate change, but can provide a more accurate understanding of how individual organisms will be impacted by shifting environmental conditions within their natural habitats.
So does this all mean that we shouldn’t worry about climate change? – ABSOLUTELY NOT! Climate change is currently, and will continue to be a huge problem for humans and a plethora of other organisms. However, I do think that the degree to which climate change will be a biological problem is poorly understood. On the bright side, scientists are beginning to recognize these shortcomings and are now working toward a better understanding of how climate change will affect marine organisms. Furthermore, not all studies simply employ highly controlled laboratory experiments; there is field evidence that provides sound information regarding the biological effects of climate change for some species. Ultimately, stamp collecting gets us nowhere – experimental approaches need to incorporate multiple shifting stressors and their associated variability, as well as numerous species (optimally mimicking communities or ecosystems) in order to adequately understand the biological implications of a changing climate. Until then, we will likely remain naive about the ways in which climate change will impact marine species.
It’s a story that many of us know well; a charismatic, touching and often hilarious tale of a father’s relentless pursuit to find his lost son. In Disney-Pixar’s 2003 blockbuster, “Finding Nemo”, a young clownfish by the name of Nemo ventures off into the open ocean, is unfortunately captured by humans, and is sent off to reside in a dentist office fish tank in Sydney, Australia. As a result, Nemo’s father, Marlin, with the company of his newfound pal, Dory, sets off across the big blue ocean to find his son and bring him home, while Nemo frantically plans his escape from the dentist office fish tank. After much hullabaloo, including Marlin and Dory encountering a hungry shark and a humpback whale, Nemo eventually escapes the dentist’s office and catches up with his dad (who unfortunately thinks Nemo is dead) and together with Dory they head for home – a touching story indeed. Though the ending is certainly of the feel-good genre, would the story have turned out the same in an acidified ocean?
Ocean acidification is a process whereby increasing atmospheric CO2 dissolves into the oceans, lowering their pH and making them more acidic. Though calcifying organisms are thought to be among the most negatively impacted, research has also suggested that an increasingly acidifying ocean can impair the behaviour of various marine fishes, with coral reef fish being the most intensively studied. Furthermore, among the coral reef fishes that have been studied, clownfish (Amphiprion percula) have been a fairly popular species of interest.
In 2010, Danielle Dixson and colleagues reported the results of their research comparing the ability of juvenile clownfish to avoid their predators under both ambient (present day) and elevated (2100 projection) CO2 conditions. What Dixson et al. (2010) found was that, in comparison to fish raised in present day CO2, juvenile clownfish reared under elevated CO2 were unable to distinguish between predators and non-predators, spending equal amounts of time hanging around both (though newly-hatched larvae were unaffected; Figure 2A). Likewise, Simpson et al. (2011) reported that clownfish lost their ability to avoid the sounds of their predators when raised under elevated CO2 conditions (Figure 2B). Additionally, negative impacts on the homing ability of clownfish have also been reported. Munday et al. (2009) found that baby clownfish raised under elevated CO2 conditions lost the ability to choose their preferred and optimal habitat and were also unable to distinguish their parents from other clownfish (Figure 2C).
These negative changes in clownfish behaviour are likely induced by a change in their biochemistry when reared under elevated CO2 conditions. Studies have suggested that high levels of CO2 interfere with one particular chemical in the brains of fishes (and other animals as well) – GABA (chief inhibitory neurotransmitter vertebrate central nervous systems; e.g. Nilsson et al. 2012). Since the GABAA receptor has a specific conductance for Chlorine (Cl−) and bicarbonate (HCO3−) – the two ions most likely to be impacted under elevated CO2 conditions – this explanation seems probable.
So how would this have impacted Finding Nemo? Well, if we revisit the plot of the movie, there are two ways in which acidification may have changed the outcome of Finding Nemo. Firstly, in the original movie, Marlin and Dory swim away when they come across a predatory shark (though shark odour tracking may also be hindered in a more acidified ocean; see Dixson et al. 2014). However, in a more acidified ocean, as research has suggested, they may have done exactly the opposite and would likely have become dinner for the shark. Secondly, at the end of the movie, Nemo pops out of a sewer pipe and swims along, eventually finding his dad and Dory. Unfortunately, in a more acidified ocean, research suggests that Nemo likely wouldn’t be able to find his father.
Though I like to think that adult behaviour may not be altered and Marlin would have eventually found the dazed and confused Nemo (though other inaccuracies in the movie, if corrected for, would have led to Marlin and Dory’s demise, let alone a much more incestual tale), it is likely that the feel-good ending that we’ve all come to love would have been anything but feel-good. So we need to find ways of mitigating ocean acidification and saving our precious ecosystems from the myriad of destructive consequences that they will face if we continue our ways – not only for our own sake, but so that the Nemos of the future will have a chance to swim away from their predators or find their way home if they ever decide to venture away from their anemonemone.
Munday, PL et al. 2009. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. PNAS, 106: 1848-1852.
Dixson, DL et al. 2010. Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecology Letters, 13: 68-75.
Simpson, SD et al. 2011. Ocean acidification erodes crucial auditory behaviour in a marine fish. Biology Letters, doi:10.1098/rsbl.2011.0293.
Nilsson, GE et al. 2012. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nature Climate Change, 2: 201-204.
Dixson, DL et al. 2014. Odor tracking in sharks is reduced under future ocean acidification conditions. Global Change Biology, doi: 10.1111/gcb.12678.
On the need to incorporate carbonate variability parameters in predicting the biological impacts of ocean acidification
This post is published as an excerpt of a “Quo Vadimus” essay to be submitted to a special issue of the ICES Journal of Marine Science. I highly appreciate any criticisms and/or feedback on the article.
Ocean acidification is expected to yield negative implications for a wide array of marine organisms in the near future, as average oceanic pH levels are projected to drop by 0.3-0.4 units by the end of the century (e.g. Orr et al. 2005, IPCC 2014). However, as with other processes affected by global climate change, variability in oceanic carbonate chemistry can also be expected to increase. For example, precipitation and temperature are expected to become more variable in the future, while the frequency and magnitude of extreme weather is expected to increase (Easterling et al. 2007, IPCC 2014). Consequently, environmental conditions within marine habitats may become more variable, including more pronounced fluctuations in marine carbonate chemistry.
Although we can expect the variability of marine carbonate chemistry to increase in the future, oceanic pH is already highly variable both spatially and temporally, with coastal areas being the most dynamic of these systems. This variability can be primarily attributed to differences in ecosystem processes across systems. Although some studies suggest that interannual and seasonal surface ocean [CO32-] variability is negligible, except in higher latitudes (temporal and arctic regions) (Orr et al. 2005), others report fairly substantial variability. For example, a study by Dore et al. (2009) utilizing 20 years of time-series measurements suggested substantial interannual and seasonal variability, coupled with a long-term decrease in pH in the north Pacific, with seasonal trends driven primarily by changes in temperature, mixing, and the net assimilation of photosynthetic CO2. Biological processes have also been suggested to drive seasonal variation in CaCO3 saturation states in the Arctic Ocean (Bates et al. 2009), while highly variable carbonate parameters have been recorded in California current systems (Hauri et al. 2009, Lienweber & Gruber 2013). The degree of variability in marine carbonate chemistry also varies within and among systems. For example, in the North Sea, it has been reported that a low degree of pH variability exists in biologically inactive areas (< 0.2), but a high degree of variability exists in coastal areas, particularly those around the mouths of rivers (Hinga 2002, Blackford & Gilbert 2005). Likewise, in Australia, degrees of pH variability have been shown to vary temporally and spatially, but specific trends are not always evident (Gagliano et al. 2010), while substantial variation in carbonate saturation has been reported from a Great Barrier Reef flat, although the impacts of such variability on coral calcification are unknown (Shaw et al. 2012). Sediments are also known to be highly variable with respect to carbonate geochemistry, varying by different degrees both spatially and temporally (Figure 1, Wenzhöfer 1999, Yates & Halley 2006). Annual patterns in carbonate geochemical variability have also been documented to correlate with cyclical trends in the abundance of benthic organisms (i.e., foraminiferans; Green et al. 1993). Rainfall can also impose drastic changes and substantial variability in sediments (Figure 1) and coastal systems (Doney et al. 2007), with negative relationships observed between rainfall and pH (i.e., increased rainfall, lower pH).
Studies have provided a solid basis for understanding the complexities of marine carbonate variability. However, the ways in which these temporal and spatial trends (or lack thereof in some areas) will impact marine organisms at the various levels of biological organization are still unknown. Some studies have started to incorporate variability parameters into assessing the biological impacts of ocean acidification, suggesting that the effects of fluctuating carbonate chemistry are species specific, allowing organisms to adapt and persist or become more vulnerable in an acidifying ocean. A study conducted by Alenius & Munguia (2012) suggested that the intertidal isopod, Paradella dianae, although adapted to a high degree of variability because it lives in the intertidal zone, experiences behavioural and physiological changes under variable pH conditions compared to a stable, low pH environment, with variable conditions (low pH) yielding negative impacts on survival, oxygen consumption, and behaviour (significantly depressed swimming time and increased resting time). Cornwall et al. (2013) also observed significantly lower growth rates of coralline macroalgae under variable pH conditions relative to static conditions. On the positive side, Default et al. (2012) have reported beneficial effects of fluctuating pCO2, reporting increases in growth and survival of coral recruits under naturally-fluctuating levels of pCO2. Similarly, when assessing the impacts of static and variable pH (O2 was also assessed, but ignored here), Frieder et al. (2014) reported that low pH treatments incorporating variability resulted in quicker transitions from trochophore to veliger larvae and larger (and less variable) larval shells compared to static low pH conditions for two species of mussels (Mytilus galloprovincialis and M. californianus). Although they did not directly test the impacts of variability on animals, Shaw et al (2013b) have outlined to importance of carbonate variability on the exposure time of marine organisms to conditions either above or below current and projected means.
The vast majority of studies assessing the biological consequences of ocean acidification focus their efforts on organisms raised under or exposed to static conditions based on mean predicted near-future acidification scenarios (Figure 2). Furthermore, although research has started to shift toward assessing the biological impacts of near-future OA conditions in the context of other environmental factors (e.g., multiple factors; temperature, salinity, oxygen, etc.), they have yet to focus on understanding the impact of acidification on marine fauna in the context of current and future marine carbonate variability. Because carbonate variability can modulate an organism’s duration of exposure to carbonate conditions above, at, or below current and projected means, as well as increase the extremes that the organism experiences, variability may offset the negative effects of ocean acidification, or amplify them. Since the time spent in conditions yielding biological effects is likely increase over time, along with the extremes of these conditions (Figure 3, Shaw et al. 2013a), it would be expected that future marine carbonate variability would result in more pronounced biological effects. Of the four studies directly relating carbonate variability to biological effects, two suggested that variability will act to modulate the impacts of ocean acidification (Default et al. 2012, Frieder et al. 2014). However, it is important to recognize these studies use current degrees of variability as the basis for future variability, which may be inaccurate. As such, the duration and extremes of the conditions that the animals in those two studies were exposed to could have confounded their results, as the tested duration and extremes of conditions may not have accurately depicted those of actual future scenarios (Figure 3). As such, an accurate understanding of how carbonate variability will transpire in the future, along with how marine organisms will respond to current and near-future acidification is of utmost importance for understanding the true biological impacts of ocean acidification.
Although the current data on how variability around current and future carbonate geochemical means suggest that marine carbonate variability will have differential effects on different species (Figure 4) and that the magnitude of the effects of ocean acidification may be more or less pronounced under variable conditions (in comparison to static conditions), the number of studies that have attempted to address variability parameters in biological ocean acidification studies is negligible and insufficient to draw any generalizations. As such, it is critical that ocean acidification research, in the context of biological impacts, begins to understand current and projected localized and broad-scale variability in marine carbonate systems to accurately predict how organisms will respond under future acidification scenarios. It is also apparent that studies focusing on the biological impacts of ocean acidification need to begin understanding how the degree of marine carbonate variability is going to change with an increasingly acidifying ocean in the myriad of systems that will be impacted by ocean acidification. Understanding whether or not the variability in the marine carbonate system is going to increase, decrease, or remain the same under future climate change scenarios is imperative for predicting how marine organisms will respond to an acidifying and warming ocean. Ultimately, because ocean acidification studies focus on stable conditions under near-future predictions, our current understanding of how acidification will impact marine organisms is very limited, rendering it critical to begin understanding how acidification will affect these organisms in the context of variability around the projected means, as well as in the context of other environmental factors and their associated variabilities.
Alenius B & Munguia P 2009. Effects of pH variability on the intertidal isopod, Paradella dianae. Mar Freshw Beh Phy, 45, 245-259. doi: 10.1080/10236244.2012.727235.
Bates NR et al. 2009. Ocean acidification and biologically induced seasonality of carbonate mineral saturation states in the western Arctic Ocean. J Geophys Res, 114, C11007. doi: 10.1029/2008JC004862.
Blackford & Gilbert 2005. pH variability and CO2 induced acidification in the North Sea. J Mar Sys, 64, 229-241. doi:10.1016/j.jmarsys.2006.03.016.
Cornwall CE et al. 2013. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc R Soc B, 280, 20132201. doi: 10.1098/rspb.2013.2201
Default AM et al. 2012. Effects of diurnally oscillating pCO2 on the calcification and survival of coral recruits. Proc R Soc B, 279, 2951-2958. doi: 10.1098/rspb.2011.2545
Doney SC et al. 2007. Impact of anthropogenic atmospheric nitrogen and sulfur deposition on ocean acidification and the inorganic carbon system. Proc Nat Acad Sci, 104, 14580-14585. doi: 10.1073/pnas.0702218104.
Dore JE et al. 2009. Physical and biogeochemical modulation of ocean acidification in the central North Pacific. Proc Nat Acad Sci, 106, 12235-12240. doi: 10.1073/pnas.0906044106.
Easterling WE et al. 2007. Food, fibre and forest products. In: Climate change 2007: Impacts, adaptation and vulnerability (eds. Parry ML et al.), pp. 273–313. Cambridge University Press, Cambridge.
Frieder CA et al. 2014. Can variable pH and low oxygen moderate ocean acidification outcomes for mussel larvae? Glob Change Biol, 20, 754-764. doi: 10.1111/gcb.12485
Gagliano M et al. 2010. The basics of acidification: baseline variability of pH on Australian coral reefs. Mar Biol, 157, 1849-1856. doi: 10.1007/s00227-010-1456-y.
Green et al. 1993. Carbonate dissolution and temporal abundances of Foraminifera in Long Island Sound sediments. Limnol Oceanogr, 38, 331-345.
Hauri C et al. 2009. Ocean acidification in the California current system. Oceanogr 22, 60-7. doi: 10.5670/oceanog.2009.97
Hinga RH 2002. Effects of pH on coastal marine phytoplankton. Mar Ecol Prog Ser, 238, 281-300.
IPCC 2014. Climate change 2014: impacts, adaptation and vulnerability. Contribution of Working Group II to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press.
Lienweber A & Gruber N 2013. Variability and trends of ocean acidification in the Southern California Current System: A time series from Santa Monica Bay. J Geophys Res, 118, 3622-3633. doi: 10.1002/jgrc.20259.
Orr JC et al. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature, 437, 681-686. doi: 10.1038/nature04095.
Shaw EC et al. 2012. Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J Geophys Res, 117, C03038. doi: 10.1029/2011JC007655.
Shaw EC et al. 2013. The role of CO2 variability and exposure time for biological impacts of ocean acidification. Geophys Res Lett, 40, 4685-4688. doi:10.1002/grl.50883.
Wenzhöfer F 1999. Biogeochemical processes at the sediment water interface and quantification of metabolically driven calcite dissolution in deep sea sediments. PhD dissertation, University of Bremen, Germany
Yates KK & Halley RB 2006. Diurnal variation in rates of calcification and carbonate sediment dissolution in Florida Bay. Estuar Coast, 29, 24-39.