Dr. Karen Maruska interview

PictureDr. Karen Maruska

I promised when I started the blog that I would bring you interviews with professionals from all aspects of fish keeping. Even though I am an amateur aquarist and this blog is for hobbyists, science regularly informs the hobby. Therefore, let me introduce Dr. Karen Maruska. She is currently an Assistant Professor in the Department of Biological Sciences at Louisiana State University (LSU). She received her B.S. from University of New Hampshire, M.S. from Florida Tech, Ph.D. from University of Hawaii, and postdoc at Stanford University. Her research uses fishes as vertebrate models to study how the brain controls social behaviors such as reproduction and aggression.​All photos courtesy of Karen Maruska.

​Let’s get started.

​The Cichlid Stage: Your research revolves around fish, especially cichlids. How and/or why did you become interested in conducting research on fish?

I’ve had a fascination with fishes since I was a kid. Growing up, I had fish tanks, did lots of fishing, and constantly begged my parents to go to aquariums. In school, I used every opportunity for class projects to do something with fish. In 7th grade, I used my mom’s fish-shaped pan to create a paper-mache fish mold and then used random objects to recreate all of a fish’s internal organs inside it. Then in 9th grade, I convinced my Earth Science teacher to let me write a paper about great white sharks! My first real research opportunity in fish biology was in college when I worked in a lab that studied lampreys and salmon. Since then, I’ve worked on a variety of different fishes including sharks and stingrays, gar, toadfish, coral reef fishes such as damselfish, gobies, butterflyfish, wrasses, and now freshwater African cichlids.

Fishes are the largest and most diverse group of all vertebrates, with >30,000 different species. They are valuable models to answer many basic biological questions for several reasons.

​First, they show incredible diversity in their behaviors, reproductive strategies, feeding techniques, and sensory abilities. This means, for example, if you want to better understand something like how parental care behaviors might have evolved, there are closely related cichlid species that show a variety of parental strategies, such as mouth brooding, substrate care, maternal, paternal, and biparental care, for comparisons. For my research, I was specifically interested in how the brain makes decisions during social interactions, and cichlids exhibit some very well-characterized and tractable aggressive and reproductive behaviors to work with.

Second, many fishes, and cichlids in particular, are relatively easy to manipulate (e.g., put in different social contexts) and breed and maintain in the lab, allowing us to address biological questions on everything from whole animal behavior down to subcellular molecular mechanisms. The genome of several African cichlid species has also been sequenced, allowing us and other research labs to study links between behavior and gene expression. Further, because they are vertebrates, with many aspects of their anatomy and physiology that are similar to other animals, including humans, research on fishes often has important implications for many scientific fields including conservation and biomedicine. As an example, some of our current research is focused on understanding how the brain controls behaviors during mouth brooding, which has implications for understanding eating disorders in humans.

Females care for their developing young inside their mouths for about 2 weeks, during which time the mother does not eat, shows signs of weight loss, and has a distended jaw as the fry grow larger.

In our study species Astatotilapia burtoni (formerly Haplochromis burtoni), females must eat a lot to put energy into growing their eggs, but once they spawn and hold the fertilized eggs in their mouth, they must stop eating immediately so they don’t consume their own offspring. These females then don’t eat during the ~2 week brood period, and then once releasing the free-swimming fry, must begin to eat again quickly to prevent death from starvation. How does the brain control this rapid switch between feeding and maternal care behaviors, and help the female survive the 2 week period of starvation? If we can discover some of the mechanisms involved in curtailing or promoting the motivation to eat, it may provide insights into the neurological control and treatment of eating disorders.

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Mouth brooding females will take up fry into their mouths when threatened during a few day period of maternal care after fry release.

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Dominant male A. burtoni are brightly colored yellow or blue with a distinct black eye-bar and red humeral patch near the gills and sometimes on the head.

​TCS: Following up on that, please describe your research to the readers.

My lab is interested in how the brain integrates information from external social signals and from an animal’s own internal physiological state to produce appropriate behaviors. In other words, how does the brain control specific behaviors associated with aggression and reproduction? Our work seeks to understand how an animal processes information from its social environment, which is often delivered in multiple sensory channels, and then translates it into context-specific behaviors used for survival and reproduction. Right now we are doing a lot of work looking at which neurons in the brain are activated when fish are placed in different social contexts, and where in the brain information from different senses might be analyzed and used to make decisions about whether to fight or to flee, or to eat or take care of developing offspring, or to be aggressive or reproduce. Some of our current projects include understanding the effects of anthropogenic noise on behavior, physiology, and hearing, the role of chemosensory communication during reproduction, the role of visual and acoustic information during mating, and the neural control of mouth brooding and maternal care behaviors. To address these questions we use lots of different techniques, and have lots of help from research associates, graduate students, undergraduate students, and collaborators from other Universities.

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The fish room in the Maruska Lab for housing and breeding the colony of Astatotilapia burtoni used for research. The system was designed by Aquaneering and includes automatic dosing systems for buffer and salinity, controlled LED dusk to dawn lighting, and web-based monitoring of all water parameters.

For more information and to follow our research progress, you can check our lab website and the LSU College of Science blog post (with video) about our research program. You can also follow us on twitter @MaruskaLab.

http://www.kmaruska.biology.lsu.edu/
http://lsuscienceblog.squarespace.com/blog/2016/10/30/its-all-about-braiiinnnssss-in-karen-maruskas-fish-lab

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Research in the Maruska lab is focused on studying the brain in cichlids to better understand how animals communicate and how behavioral decisions are made during different social contexts such as aggression and reproduction.

​TCS: As you mentioned, some of your research focuses on how sensory input affects fish behavior. If there is any one environmental factor, such as temperature, pH, sound, or light, that has the greatest influence on behavior, particularly when the factor varies, which one would it be and why?

I think all of these factors can potentially affect fish behavior in some way, and of course the effects can differ drastically among different species, with some species more tolerant to environmental fluctuations than others. From my own experience using Astatotilapia burtoni in the lab, temperature has big effects on behavior. We have had several instances where the temperature in our fish facility has dropped ~10 degrees, and the fish do not behave normally; they are slower, perform fewer reproductive and territorial behaviors, and show more signs of stress. Temperature can have wide-ranging effects on fish physiology by influencing the activity of nerves and muscles, among other things.

Cichlids are very visual fish, so light conditions that reduce visual abilities can also affect their behaviors. However, we’re now discovering that cichlids are more multimodal (use many different senses) than previously thought. For example, during communication, many species also make sounds, create water movements that are detected by the lateral line system, and can signal to each other through release of chemical compounds (via urine & feces, or passively released through gills & skin) that can be detected by olfactory and taste systems. They also likely use a combination of sensory cues (visual, acoustic, smell, taste) to find food and evade predators. Because they rely on many senses, they are at an advantage if one sensory channel becomes inefficient due to changing environmental factors such as lighting or pH or acoustic noise, and can switch to using a different sensory cue to survive in different conditions. For example, in the presence of acoustic noise, fish may increase visual or chemosensory signaling, and in visually turbid conditions, fish may rely more on making sounds or sending pheromones through urination. While this ability to quickly adapt to changing environmental conditions allows them to survive in their natural habitats, it unfortunately also likely contributes to the successful establishment of many cichlid species (such as tilapia) that are now invasive in many parts of the world.

The effects of pH on fish behavior has been a hot topic recently because the atmospheric carbon dioxide levels are on the rise due to global warming, which is lowering the pH levels (making more acidic, or less alkaline) in our oceans. Several recent studies have shown detrimental effects of low pH, high carbon dioxide conditions on fish behavior, which can affect their cognitive abilities used to find food, navigate, find mates, and escape from predators. There is also some evidence in cichlids and other fishes that factors such as pH and temperature will affect sex ratios (number of male vs. female offspring) and expression of alternative reproductive phenotypes within a population. So, varying environmental parameters can also have widespread effects beyond sensory abilities that ultimately impact species persistence.

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In addition to visual signaling, many cichlids also communicate by releasing important compounds in their urine (left) and making sounds (right). In Astatotilapia burtoni, both males and females release urine (visualized by injection with an innocuous blue dye, arrow) in aggressive and reproductive contexts. Dominant males also produce pulsed low frequency sounds during courtship quiver behaviors to attract females. [From Maruska & Fernald 2012; Maruska et al. 2012].

​TCS: You have conducted considerable research on the lateral line in fishes. Can you describe for the readers what this is and the role it plays?

The lateral line system helps fish detect water movements around their bodies. It’s often a difficult sense for people to understand because humans don’t have it, but it’s really important for fish. It’s found in all fishes and aquatic amphibians, and functions in behaviors such as schooling, prey detection, predator avoidance, social communication, obstacle avoidance, and rheotaxis (orienting in water currents). The basic units of the lateral line system are called neuromasts, which are groups of sensory hair cells (similar to those found in the inner ear used for hearing and equilibrium) and support cells covered be a gelatinous structure called the cupula. These neuromasts can be found either on the skin surface (superficial neuromasts), or located within enclosed canals that have pore openings on the skin surface (canal neuromasts). When the cupula is deflected by water movements around the fish, it essentially stimulates the underlying hair cells, which then send signals down a nerve into the brain, providing the fish with some important information about the source of the movement. These superficial and canal neuromasts are found both on the head and along the side of the fish, but the distribution pattern varies depending on the species.

Determining the exact contribution of the lateral line system during different behaviors is notoriously difficult because it is hard to block or knock out the system without inadvertently affecting other sensory systems, such as olfaction or hearing. Without the ability to selectively eliminate only the lateral line system, it is difficult to know for sure whether certain behaviors depend on this sense. Nevertheless, our recent work has demonstrated that water movement cues sensed by the lateral line system are important during aggressive contests in A. burtoni. Male-male fights typically begin with several non-contact behaviors such as lateral displays and frontal threats, which involve the two fish pushing water at each to assess the size, fitness, or fighting ability of their opponent. When the lateral line system is blocked, males perform more damaging contact behaviors such as biting, ramming, and mouth fighting because they are unable to safely assess each other without detecting the water movements generated via non-contact behaviors. This is some of the first experimental evidence that the lateral line system is indeed involved in social behaviors, and it is likely used during other social interactions such as mating and parental care.

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The lateral line system in the cichlid Astatotilapia burtoni. A) Structure of a single neuromast, the functional unit of the lateral line system. B) Distribution of canals, canal neuromasts, and superficial neuromasts on the head and body. C) Labeling of neuromasts (green dots) in A. burtoni with a fluorescent dye. [From Butler & Maruska 2016].


​TCS: One of the great joys of cichlid keeping is the fact that they often have individual personalities. What are some of the biggest behavioral surprises that you’ve encountered in your research?​

I am constantly amazed by the individual variation in behaviors of our cichlid population! When I first started working on A. burtoni, the behavior that was most striking to me was how quickly a subordinate male in the population can take over a vacant territory and begin performing the aggressive and reproductive behaviors typical of the dominant male phenotype within just a few minutes! If we removed a dominant male from his territory, within a few minutes, the next ranking subordinate male in line would brighten his colors, turn on his eye-bar, and begin courting females and chasing away rival males. This rapid change in behavior is also associated with quick physiological changes from the brain down to the testes, which helps the male transition to a reproductively dominant territory-holding male. It is also always surprising to see subordinate males in a community tank that will turn on their eye-bar and perform aggressive behaviors or court a female only when the resident dominant male is inside his shelter or isn’t looking, and then stop and turn off their eye-bar when the resident comes back into view. It’s remarkable how aware these fish are of their social surroundings and that they can be just as ‘sneaky’ as humans in certain situations!

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A dominant male Astatotilapia burtoni flaring his fins and opercula as part of a threat display. Also note the egg-spots on the anal fin that are used during courtship and spawning in this species.

​TCS: Many hobbyists believe that, in order to thrive in aquaria, cichlids require water parameters (e.g, pH, hardness) that closely mirror their endemic environment. Is that really true for cichlids that are captive bred (perhaps in municipal or well water that is more neutral) and multi-generations removed from their native water? Could you explain?

It is possible that cichlids bred in captivity will over time become more tolerant and adapt to certain water parameters, but I think this likely varies quite a bit depending on the species and the limits of their physiologies. Cichlids are champions of rapid adaptation and evolution of traits to better survive in changing conditions, so it’s also theoretically possible to select for individuals in a population that better survive, for example, in a different pH, temperature, or salinity. In general though, I still think there are optimal water conditions that allow cichlids to thrive, behave naturally, and breed in aquaria. I also think that mimicking the habitat they naturally inhabit in terms of temperature, lighting regime, pH, and salt composition is the best way to ensure their survival and maintenance of typical behaviors and coloration patterns for longer periods of time.

TCS: You’ve conducted research on the effects of acoustic communication in the reproduction process. I’ve always felt that extraneous noise (e.g., from filters, air stones, powerheads) in a closed system like an aquarium has to have some kind of impact on fish, and probably a negative one at that. Can you comment on the potential short-term and long-term effects of man-made, perpetual noise on captive fish?

Great question! I agree that constant noise likely has negative impacts on fish, and we are actually studying this right now. One of my graduate students is examining the impacts of human-generated noise on cichlid behavior, physiology, and hearing abilities. Using loud noises, she has already revealed several important negative impacts. For example, noise alters how males fight and defend their territories, and destroys hair cells in the ear, which likely impairs hearing abilities. In the mouth brooding females, excess noise negatively affects their ability to successfully brood their young, and the fry exposed to noise in the mother’s mouth have higher mortality and slower growth rates. I need to point out, however, that these experimental effects are due to much louder noises than would typically come from aquarium noise such as filters and air stones. But, there are also likely other subtle effects on hearing, behavior, and physiology (e.g. stress) from the constant lower intensity sounds caused by aquarium filtration. Since the sounds from aquarium equipment are also usually within the low frequency range (<~1500 Hz) of fish hearing, the chances for detrimental effects are higher. In fact, there is evidence in the literature for these types of effects in several different fish species.

TCS: One characteristic cichlids are known for is aggression. Do you have any pointers for helping hobbyists predict such behavior before it truly becomes a problem or mitigate it when it does?

PictureDominant males often push water at each other with flared fins and opercula during territorial aggressive behaviors. These water movements can be detected by the lateral line system.

It is difficult to predict excess aggression ahead of time, but the best thing to do is watch each individual fish in the tank frequently and look for signs of aggression. This can be either overt behavioral displays like chases, bites, rams, etc. from the aggressor or frayed fins, missing scales/wounds, or subordinate behaviors from the recipient. Since the majority of aggression is performed by males, it’s usually a good idea to have 2-3 females per male to help reduce repeated aggression on a single individual. Ideally, if aggression escalates to the point of injury, the best option is to move the aggressor to another tank (or the recipient of the aggression if one particular fish is being picked on), although I know most home aquarists might not have this luxury. An alternative option is to put a divider (e.g. clear acrylic or fine mesh netting) somewhere in the tank to separate different groups of fish to see if you can establish a more socially stable environment since they can still interact across the barrier, but not physically hurt each other.

PictureTwo dominant males (blue and yellow color morphs) fight over the border of their adjacent territories by performing aggressive behaviors such as frontal threats, lateral displays, and border fights.

Another thing that helps temper excess aggression is making sure there is enough habitat with shelters and places to hide for all of the fish in the tank, as well as enough food to reduce competition for this resource. As you know, most cichlids are naturally aggressive to some extent, and I have also seen huge variation in aggressive behaviors among different individuals – some fish are always looking to pick a fight no matter who they’re placed with, while others are more passive and happy in any social environment. The key is to establish an environment that allows display of their natural aggressive behaviors, without compromising their health and well-being.

TCS: Do you have any advice for creating a socially stable, African cichlid environment?

I think the answer to this will vary depending on the species involved. In A. burtoni, the key is to have a good mix of both males and females that are of similar sizes, and to monitor their behaviors and territory establishment over time in order to intervene when one fish becomes too aggressive. In my experience, providing enough space and complex shelter (rocks, logs, plants, etc.) for all of the individuals in a community is also very important. Having suitable substrate like gravel, rocks, or sand for species that dig spawning pits or build bowers will also help to keep them busy.

I don’t have much experience with mixed species cichlid communities, but some of the same considerations above seem to hold true. Of course, always choose species that are compatible in temperament and behavior so they can establish their own niche in the environment. Since cichlids will very quickly establish territories and a social hierarchy among the individuals, it’s also important to introduce any new individuals carefully into an already established tank. Some strategies I know that have worked for others include introducing new fish at night when fish are not aggressive, or to rearrange the structures and shelters in the tank before adding new fish so the residents become preoccupied with regaining a territory and pay less attention to the newcomer. Occasionally reorganizing the aquascape can be used as a strategy to curtail aggression as well.

TCS: As you’ve already mentioned, the model organism for your research is the Astatotilapia burtoni from Lake Tanganyika in Africa. If you could choose another couple of cichlid species as your models, what would they be and why?

There are so many interesting cichlid species and different ones would be ideal for different types of research questions. One group that I think are particularly cool are the Princess cichlids like Neolamprologus brichardi/pulcher from Lake Tanganyika. They have really complex social structures including group living and cooperative breeding behaviors, so it would be interesting to explore the sensory and neural processing mechanisms of this cooperative behavior. They also have a sequenced genome and are relatively easy to maintain in the lab, so conducting studies on behavior and molecular mechanisms are possible.

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