why we should eat insects

   I have not done it very much, but I am an advocate of eating insects. The first time was in my Entomology class in college, almost 20 years ago. My professor, Dr. Letourneau, sautéed some butter and garlic at the front of the classroom, dropped in a container of mealworms (which are actually beetle larvae, not worms at all), and served them with slices of baguette. It was good. Butter and garlic can make anything taste good. I also ate escamoles, an ant egg delicacy from Central Mexico.

Liometopum occidentale, one of two ant species whose eggs are harvested for escamoles (Image credit: Michael Branstetter 2007, AntWeb.org)

   
   During a work trip to Querétaro, Mexico my colleague introduced me to escamoles at a fancy Italian restaurant – they were not on the menu and I had no idea how much they cost. The ant eggs were cooked in spices and served alongside corn tortillas and guacamole and made into little tacos. Biting into the taco was superb, the texture worked and the flavor was unlike anything I had eaten before. There was a subtle popping with each chew, and the flavor of the eggs resembled that of buttery pine nuts. I have also had brownies with whole crickets embedded in the top. Is there more of a grossness factor when you can see and recognize the entire insect as it goes in your mouth? Yes, it made my stomach flutter. But the escamoles did not affect me at all, and the mealworms only a little.    

   Insects are traditional foods (and often delicacies) that are eaten regularly in Latin America, Africa, and Asia. The same cannot be said for the United States. Finding insects in the store or at a restaurant is rare. But it doesn't have to stay this way; Americans have overcome culturally-based food obstacles in the past. Let us consider the history of lobster in the United States. There was a time when New Englanders fertilized their gardens with lobsters, and eating them indicated things were not going well for you financially. So what are the barriers preventing this from happening with insects? I haven’t collected any data but I think it is safe to say that many Americans think it is just plain gross. How appealing does eating a whole cricket, or mealworm, sound to you? I don’t disagree. And I don’t think you and I are alone, which is why companies have started marketing insects in unrecognizable forms. Cricket flour, dry roasted crickets ground up into a fine powder; and mealworm tofu. We can also overcome this obstacle by thinking about eating insects and lobsters from an evolutionary perspective. Insects and lobsters are in the same evolutionary lineage called Arthropoda - they are very closely related. So much so that insects could be considered a terrestrial version of lobsters, crabs, and shrimp. So, biologically speaking, eating insects is no different than eating lobster.

   Why am I talking about eating insects? What does this have to do with scientific discoveries? Since I study insects I spend a lot of time thinking and reading about them in different contexts. One of those contexts is eating them, and it is impossible to overstate the benefits. As established by the United Nations Food and Agriculture Organization (FAO), consideration of insects as a critical food source is essential because they are 1) highly nutritious, 2) an important component of traditional diets in food insecure regions, and 3) environmentally sustainable relative to alternative protein sources such as beef. In addition, eating insect pests can reduce pesticide use with added economic incentives. Researchers in Mexico have developed a strategy to harvest a Mexican grasshopper pest from crops using mechanical methods (rather than pesticides) that would result in a gross income of US$350 million annually if the crickets are subsequently sold for human consumption.

   Because all of these factors can positively impact the health of our planet and its population for the long term, my plan is to come up with some good recipes and integrate insects into my diet. So I bought some cricket flour. I used it to make pizza dough. And as much as I want to tell you how successful my first try was, I can’t. Let me explain. I like to cook; and while I am no culinary genius, there is some culinary talent in my family. I have a basic understanding of flavors and flavor combinations.

Cricket flour (I am not sponsored by this company in any way and am not advocating for purchase of this particular flour)

    
   The cricket flour was brown and had an earthy, soil-like aroma. It tasted a lot like soil as well. I have read some articles describing cricket flour as nutty - I didn’t get nutty, just earthy. Since earthy falls in the savory category, I decided to make a savory dish rather than something sweet as many people suggest. I chose pizza dough.

Cricket flour pizza dough

    
   I followed the recipe of a simple pizza dough from my favorite food blog, Smitten Kitchen. It seemed small so I doubled it. Instead of adding three cups white flour I added two cups white flour, ¾ cup cricket flour, and ¼ cup whole-wheat pastry flour. To counteract the earthy, bitter flavor of the cricket flour I topped the pizza with caramelized onions. One half had olive oil, caramelized onions, and Trader Joe’s honey goat cheese; the other half had red pizza sauce, caramelized onions, and cheddar cheese. 

Left: goat cheese and caramelized onions. Right: red sauce, caramelized onions and cheddar cheese.

   
   My husband (J) and I were the judges of the cricket flour pizza dough experiment. I am not a picky eater, the only thing I will not eat is raw celery. J is even less of a picky eater and will ravenously eat almost anything.

  After my whole introduction about how healthy and sustainable it is to eat insects, you can imagine my disappointment when I did not like the cricket flour pizza dough. My initial optimism was very high. For the first couple of chews I didn’t notice a difference, especially for the half with red sauce and cheddar cheese. But as I kept chewing and swallowing, the aftertaste set it in. So earthy, too earthy. The honey goat cheese side was even more difficult, it didn’t have any sauce to overwhelm the earthy flavor. I kept trying to clear my mind and have another bite. I really wanted to love it. I wanted to be able to sit down and write about how great it was and advocate for it like nobody’s business, but my disappointment was real.

I couldn't bring myself to eat the crusts

   
   J liked it and helped himself to seconds. Maybe his disconnection with the preparation process made it easier for him? The other upside was the nutritional improvement. In one slice of pizza, the cricket flour pizza dough had 8.4 grams of protein compared to 1.6 if I had made it with all white flour. It also had 60% of the suggested daily amount of vitamin B₁₂, of which white flour has none.

   Don’t worry, I am not giving up. In the spirit of George de Mestral, and all of the other curious experimenters out there, I will keep trying. I will compare different cricket flours, and I have more recipe ideas. I will also experiment with other insect food products, like the mealworm tofu. This is not the end of insect eating for me - I have only just begun - and I will continue to be an entomophagy advocate.

commentary: evolution, bioinspiration, and biomimicry

   I am doing something a little different this week. Instead of investigating the foundational work underlying a biological discovery, I am going to talk about the difference between bioinspiration and biomimicry in the context of evolution. These are terms that have come up in previous blogs, and understanding the implications of each is both interesting and important.

Spiny-headed worms inspire. Roohi & Sattari (2015) Image caption: Fig. 2. P. laevis recovered from S. cephalus intestine stained with acetocarmine.

    Last week I engaged in some enlightening intellectual banter with one of my dear friends from college. She is a social scientist and I am an evolutionary biologist, and so it goes without saying that we are exposed to different literature, experiences, and applications of our research. One thing that came up during our conversation was whether there was directionality to evolution. We were talking about human evolution specifically but I, of course, was drawing on my own work studying evolution in beetles. Evolution by way of natural selection, as posited by Darwin and Wallace, can only operate on the variation present in a population at any given time. If we put this in terms of my favorite reality TV show, So You Think You Can Dance, it would go something like this. During the tryouts, the only option the judges have is to move someone to the next round or eliminate them. The judges cannot pick the feet of one contestant, add them to the legs of a second contestant, and then move the chimera to the next round. They must work with the variation at hand and either send a contestant to Vegas or send them home. Evolution is also much more dynamic, mostly due to the constantly changing environment organisms live in. Trait A, which may be favored most of the time, gives way to trait B during drought conditions.

Darwin, Charles (1845) Journal of Researches into the Natural History and Geology ofthe Countries Visited During the Voyage of H.M.S. Beagle Round the World (from1832-6). Under the Command of Capt. Fitz Roy.

   In other words, just because a bird beak has been evolving for millions of years, it doesn’t mean it is optimized. There is no optimum in evolution. What was optimal 100 million years ago may no longer be optimal now, but it may be 100 million years in the future. Just like bell-bottoms were high fashion in the 70’s, but definitely not in the 80’s. Then they made a comeback in the 2000’s, went out in the 2010’s, and may be coming back now (maybe, mom?) [2/23/16 update from my mom - they are now called flares].

   What does this have to do with bioinspiration and biomimicry? Many biologists, engineers, and bioengineers prefer the term bioinspiration over biomimicry because they feel it more accurately portrays the process of evolution. Biomimicry implies that we can mimic an optimal biological solution to a societal problem. But if we do that we are selling ourselves short because, from an evolutionary perspective, there is no optimal solution. As an engineer, you can take feet from one contestant and add them to the legs of another and generate a product that was inspired by nature, but not an exact mimic. Is this a matter of semantics? Maybe, but I think the distinction is important. Not just to have something to blog about, but to really try and understand the evolutionary process. And, to use that understanding to the benefit of our society by developing solutions to hard problems. Some organisms have already evolved adaptations to some of our problems, so why not take their millions of years of experience and break free from the constraints of natural selection? We are not limited by the variation currently at hand, and we shouldn’t let our curiosity be either.

spiny-headed worms: interesting enough for round two

   To delve deeper into the spiny-headed worm story we must first understand the proboscis. The proboscis is a tubular body part that sucks. A butterfly’s tongue that sucks nectar out of flowers is a proboscis. An elephant’s trunk is often called a proboscis. And the spiny sucking apparatus of acanthocephalan worms is a proboscis. 

Close-up of butterfly proboscis (image credit)

   The proboscis in parasitic worms has two functions, to attach to the host and extract nutrients from the intestinal lining. The crazy thing about the proboscis in this particular group of worms is that it is biphasic; it can be tube-like and erect, or it can be flaccid and turn itself outside-in and retract within a compartment of the worm body. When R. A. Hammond started working on Acanthocephalus ranae, our spiny-headed worm friend from last week’s post, it was known that the proboscis could retract, or invaginate. What wasn’t known was how it actually happened. Thus, the goal of R. A. Hammond’s study was to identify the in-and-out mechanism of the proboscis. Let me just say here that up until this point I have tried not to use words suggestive of a penile erection. It is a little difficult because I am talking about a tube-like structure that swells and becomes erect to function, only to return to a flaccid state when not being used. But, it is important to understand that I am not avoiding this comparison because I am afraid to talk about genitalia; on the contrary, I talk about genitalia on a daily basis. I am avoiding this comparison because it is misleading. The main difference is that when a human (or mammalian) penis becomes flaccid it does not invaginate, it just goes limp. To invaginate, the tip would have to retract in on itself and rest within an internal receptacle. Interesting idea, right? This is how many animal penises operate, from insects to reptiles. Evagination for operation, invagination for daily life. Now that we have this out of the way, let’s move on.

   To figure out how the proboscis worked, Hammond used a technique first described by Pflugfelder in 1949. Pflugfelder! I am not going to go on a tirade about him, I want to focus on Hammond, but what a name. The technique involved feeding the parasite host, in this case the common toad (Bufo bufo), pork fat with a red stain dissolved in it. Once the fat/red stain solution was in the toad’s digestive system the parasites fed on it too. The stain was sequestered in particular structures of the worm called lemnisci, which were hypothesized to be involved with the evaginate – invaginate process. I know, lemnisci is not a term I use on a regular basis either, I’ll try not to let it contribute to confusion. To summarize, Hammond fed toads a fat/red stain mixture, dissected the intestines out of the toad, pulled out the worms, imaged the stained lemnisci under the microscope using still pictures and video, and traced the morphological changes from beginning to end. All of this to find out how the worm proboscis worked. Not to invent microneedles, not to develop a surgical adhesive, he wanted to know how it worked.

   What Hammond discovered was that the invagination and evagination mechanism was controlled by a set of muscles that pulled and pushed the proboscis into and out of the receptacle by changing the hydrostatic (fluid) pressure of various morphological components. Interestingly, once the proboscis was fully extended, a set of collar muscles around the base contracted and pushed fluid up into the proboscis wall causing the skin to swell. It was this swelling mechanism of the worm that inspired the microneedle adhesive.

Figure 1a from Yun Yang et al. (2013). Image caption: "Illustration showing mechanical interlocking of a water responsive shape-changeable microneedle following penetration into tissue."

I want to point out that the microneedle adhesives were inspired by the proboscis (bioinspiration) as opposed to mimicking the proboscis (biomimicry). The reason is that the swelling mechanism of the worm proboscis relies on muscular contraction whereas swelling of the microneedles occurs with the addition of water. What is similar is that they are biphasic, and have a tip that swells relative to a base that does not. A patent application for this discovery was filed on Nov. 26, 2015. Since the original publication describing swellable microneedles, there have been several other useful applications including designs to deliver drugs, vaccines, and insulin directly through the skin.

A side note: In light of what is going on with the water supply in Flint, Michigan, I wanted to also mention how P. laevis and its relatives can be used as bioindicators in freshwater ecosystems. Because P. laevis parasitizes freshwater fish, it has been shown they accumulate heavy metals, such as lead, from the aquatic environment and can be used to monitor heavy metal concentrations. Maybe we should send some to Flint.

from spiny-headed worms to swellable microneedle adhesive

     My post on Velcro featured a plant inspired attachment discovery, and so it is only fair to counter that with a discovery of animal inspired attachment.

“There are several unmet clinical needs for adhesives to affix connective tissues including tendons and ligaments, to improve contact between tissues to reduce motion of tissue grafts, and to seal tissues for prevention of fluid (intestine) or air (lung) leaks.” (Yun Yang et al. 2013)

     In other words, society is in need of some better glue to secure different types of tissues in place after surgery. I am going to go out on a limb and speculate that surgical adhesive tape is not something many of us think about or use on a regular basis. I would also venture to guess that if one of us were scheduled for surgery, we would hope our surgeon had access to the best of the best when it came time to put us back together. Introducing Pomphorhynchus laevis, a spiny-headed worm that makes it’s living as an intestinal parasite of fish. The common name of this parasite, the spiny-headed worm, starts telling the story all on its own. To attach to a host, the worm embeds its spiny head into the intestinal lining of the fish. The head then starts to swell, preventing it from going backward, and the worm is anchored in place. Herein lies the story of an unknown fish parasite and its rise to fame as it walks the red carpet with swellable microneedle adhesives, sort of.

Image credit: Verweyen et al. (2011), Figure caption: (E) Habitus of Pomphorhynchus laevis from Platichthys flesus (Baltic Sea) shows [m]any trunk hooks on bulb, neck and trunk. Scale bar = 100 µm.

      I wanted to start our story with the original species description of Pomphorhynchus laevis (which can be abbreviated P. laevis from now on). A species description is a published narrative describing how one species is morphologically distinct from close relatives. The purpose of a species description is to anchor a name, an actual specimen of that species (known as the type specimen), and its morphological characteristics all in one publication. For example, if we think of our own species, Homo sapiens (genus Homo, species sapiens), the existence of a species description helps us classify newly discovered Homo skeletons. Are they members of our own species, Homo sapiens? Do they belong to an already described species such as the extinct Homo habilis? Or, is it a new species that has yet to be described? In fact, just last year scientists described a new species of Homo, Homo naledi, discovered near Johannesburg, South Africa. In order to identify what species the new skeleton was, scientists had to make comparisons with other Homo species using their species descriptions, and then make a case for why it was different. This can be controversial. We had enough controversy after last week though, back to parasites. In order for parasites to inspire, they first need to be discovered, named, and described; and then pursued with further investigation to see how they attach to their hosts.

     In the original publication introducing the efficacy of the swellable microneedle adhesive, the authors cited P. laevis as the inspiration for their swellable adhesive (often referred to as a biphasic adhesive, which just means two phases. Unswelled, or flaccid. And swelled). This was based on scanning electron micrographs they found when searching for parasite inspiration on the Google. But, the paper they actually reference for the worm attachment mechanism was for a different species, Acanthocephalus ranae. I emailed Jeff Karp, the corresponding author of the paper, to ask about this and he said they were inspired by the idea of swelling as a way to establish an anchor, which is used by many of these species (both are close relatives in a more inclusive group of organisms, the Acanthocephala). And, like me, they found an intriguing image of P. laevis but probably could not a find a citation for it’s attachment mechanism, and thus cited the mechanistic description of A. ranae instead.

     That may be more straightforward for our story too. In my investigation of P. laevis I found a discrepancy as to who originally described the species. Some papers cite Müller 1776 but the ITIS (an authoritative reference) lists Zoega 1776. All right already, I know I am getting very detailed about names, but this will be important and interesting as we march though a variety of discoveries so I am not editing it out. Names are important, they are the only way we can track things through time. An unnamed species is an unstudied species. At this point though, I am thinking our swellable needle story might need to be told in two parts, because you are probably losing your attention span for parasites at this point.

     Stick with me just a little longer. Acanthocephalus ranae was described by Schrank in 1788. After a little digging online I am very curious about what kind of person Schrank was. What was his life like? Why was he describing parasite species? (And not just one, it looks like there were many.) His full name was Franz von Paula Schrank (1747-1835). (Just to reinforce the importance of names, try typing Schrank into Google. Now try typing Franz von Paula Schrank. Much better.) Schrank was a German multi-tasker and is classified as a priest, zoologist, and botanist. He authored many books, all of which are old, and in German, so I am a little stumped on their content, but I did translate the titles using Google translate. Most are natural history accounts with beautiful illustrations focusing on insects, plants, and parasites. It looks like there is just one book on parasites: Verzeichniss der bisher hinlänglich bekannted Eingeweidewürmer, nebst einer Abhandlung über ihre Anverwandtschaften (Google translate: Directory of previously well bekannted intestinal worms, together with a discussion of their Anverwandtschaften), and there are only three copies worldwide. Might be a little difficult to get my hands on one. However, in 1981, Annette Zimmerman wrote a dissertation on Schrank, “Franz von Paula Schrank (1747-1835): Naturforscher zwischen Aufklärung und romantic” (Google translate: Naturalist between Enlightenment and Romanticism) that I would love to see. It is actually at the Stanford Library (QH31.S34 Z55), and I will be close to Stanford in March so I am going to try and get a look at it. We are going to learn about Schrank. But everything is in German. So it may not be soon.

Image credit

      Okay, done for today. Next week we are going to delve into the world of R.A. Hammond, the scientist who performed detailed studies on A. ranae to figure out how it attached to it’s host intestinal lining. After some searching I have not been able to find out much about him, including first name. That’s okay though, because what I would really like to do is spend some time exploring how he studied the attachment mechanism of parasitic worms, and how his studies relate to the discovery of microneedles. And there is actually a lot more to talk about with regard to the actual microneedles themselves, and the variety of tasks they have been able to accomplish since their invention.