Ocean Acidification and its Impacts on Lobster Olfactory-related Behaviors

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Winsor Watson UNH - Department of Biological Sciences Principal Investigator

I. Background and Rationale

The American lobster fishery is one of the most lucrative fisheries in the United States and it is especially important in New England. While it continues to flourish in many regions despite heavy fishing pressure, the recent near collapse of the lobster fishery in Southern New England, and declines in lobster recruitment in many areas, suggest that even slight changes in the environment can significantly impact their distribution and reproductive capacity.

While it is clear that ocean warming will likely alter the distribution of lobsters and the size at which they reach sexual maturity (Little and Watson, 2003, 2005), we know little about how ocean acidification might impact this species, as well as other commercially important marine species. Based on our own previous studies with salmon (Malmgren and Watson, 1987), and recent reports concerning the influence of acidification on fish and macro-invertebrates (see Leduc et al., 2013 for a review), we are primarily concerned that ocean acidification will interfere with the ability of lobsters and other species to detect odors, which would have: “far-reaching consequences to population dynamics and community structure” (Leduc et al., 2013). This hypothesis is based on the fact that many odorants, like the amino acids lobsters use to detect food, bind to their receptors in a manner that depends on their 3D conformation and ionic charges and these can be influenced by changes in pH.

II. Objectives

Our overall goal is to determine if ocean acidification might impact the lobster fishery by altering the ability of lobsters to mate and find food. We seek Sea Grant Development funds to gather preliminary data on this subject so that, if this line of research is promising, we can undertake a more comprehensive study of this subject in the future. Our objectives are to:
1. Determine if lobster mating behavior, which depends heavily on appropriate chemosensory communication between mature males and females, is altered when the pH of the water is decreased.
2. Determine if the ability of lobsters to locate food and consume it is impaired when the pH of the water is decreased.
3. Use neurophysiological techniques in the laboratory to determine the neural basis of pH induced alterations in olfactory-related behaviors.

III. Approach

Objective 1: Mating behavior

American lobsters typically mate ~ once/year, in the summer. Males establish and defend shelters, premolt females approach the males and both sexes release pheromones to signal that they are prepared to mate (reviewed in Atema and Steinbach, 2007). The female is then allowed to enter the shelter, she molts, and they mate. Importantly, if their olfactory systems are altered mating will not be successful. We hypothesize that low pH, due to ocean acidification, might interfere with the olfactory system and thus alter normal mating behavior.

Recently we completed two studies of lobster mating. Both were successful and the results of both studies are currently being prepared for publication. Therefore, we are well prepared to test the impacts of ocean acidification on the mating process. We anticipate that, because the interaction of the pheromone molecules with the olfactory receptors will be altered by the change in pH, male lobsters will react to females in an aggressive manner, like they do with males and immature females. If we obtain this result, then we will continue to adjust the pH in subsequent studies to determine the minimal amount of pH change (threshold) necessary to interfere with normal mating behavior. Moreover, once this value is obtained, we will determine if lowering the salinity of the water, mimicking an estuarine habitat, will change the threshold. We expect that the combination might have a greater impact on olfaction that low pH alone, because of the reduced buffering abilities of freshwater vs seawater.

Objective 2: Finding Food

The sense of smell in lobsters has been studied in some detail because of the ease of obtaining electrophysiological recordings from their primary olfactory organ, the antennules (Johnson and Atema, 1983). It appears that amino acids are the primary cues they use to detect prey and other food items (Derby et al., 1982; Zimmer-Faust, 1989). Previous studies, including our work with salmon (funded by Sea Grant), have shown that changing pH has an impact on the ability of animals to detect odors (Malmgren and Watson, 1987; Moore, 1994; see review by Leduc et al., 2013). Therefore, the hypothesis we will test is that lobsters will either be unable to detect food, or it will take them longer to find it.

A Y-maze will be used to determine if a lobster’s ability to pick the arm with the food in it will change if the pH is lowered. As in the previous experiment with mating behavior, once we obtain a reliable result we will determine the minimum pH change that will have an effect and then determine if this pH threshold is altered by lowering the salinity.

Objective 3: Neural basis of pH induced changes in behavior

If the aforementioned studies yield promising results we will study this phenomenon in more detail using extracellular recording from the antennule nerve that contains the axons used to communicate information from olfactory receptors located on the antennules to the brain. Antennules will be removed from lobsters and we will record from the antennule nerve while perfusing the antennule with seawater (Johnson and Atema, 1983). Odorants, such as amino acids or water from the vicinity of mating lobsters, will be added to the recording chamber and the neuronal responses will be quantified (changes in spike frequency). Then the pH will be decreased and the odorants will be applied a second time. Similar studies have demonstrated the impact of reduced pH on salmon olfaction (Moore, 1994). We expect the proposed studies will complement the behavioral studies and clearly demonstrate how ocean acidification might impact the sense of smell of lobsters and other marine species. Furthermore, because the lobster olfactory system is so tractable this line of research will open many opportunities for investigating, at the neural level, how ocean acidification might alter olfaction in marine species.


N.H. Sea Grant researchers determine that ocean acidification reduces lobster response to bait

In 2015, N.H. Sea Grant-funded researchers determined more acidic seawater reduces lobsters' responses to bait, indicating that ocean acidification may impact lobster populations and the commercial lobster fishery.
Relevance: Recent studies suggest that ocean acidification may impact behaviors related to the sense of smell in some marine species. Scientists are interested in determining if more acidic seawater with a low pH interferes with the ability of lobsters to detect prey or bait.
Response: In 2015, N.H. Sea Grant-funded researchers conducted laboratory studies with lobsters at two pH levels — a control level and a low pH level — and added bait. The researchers used video footage to examine lobster responses to bait and overall activity.
Results: Laboratory studies indicate that making the water more acidic by lowering the pH did not influence lobster movement, but it did reduce the response of lobsters to bait, indicating that ocean acidification impacts a lobster's ability to detect bait. These results could have implications for lobster populations and the commercial lobster fishery as climate change leads to major changes in the ocean environment.