Mealworm

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Mealworm
Temporal range: Holocene, 0.003–0  Ma
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Tenebrio molitor Linne, 1758 (32842137535).png
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Coleoptera
Family: Tenebrionidae
Genus: Tenebrio
Species:
T. molitor
Binomial name
Tenebrio molitor
Mealworms, larvae of Tenebrio molitor, illustrated by Des Helmore COLE Tenebrionidae Tenebrio molitor.png
Mealworms, larvae of Tenebrio molitor, illustrated by Des Helmore

Mealworms are the larval form of the yellow mealworm beetle, Tenebrio molitor, a species of darkling beetle.

Contents

The yellow mealworm beetle prefers a warmer climate and higher humidity. [1] Male mealworms release a sex pheromone to attract females to mate. [2]

Tenebrio molitor has been used in biomedical research. Mealworms can be a dietary source for animals and humans. [3] They are also considered pests, especially to food storage.

Description

Like all holometabolic insects, T. molitor goes through four life stages: egg, larva, pupa, and adult. Larvae typically measure about 2.5 centimetres (0.98 in) or more. Adults are generally 1.25 to 1.8 centimetres (0.49 to 0.71 in) in length. [1]

T. molitor is dark brown or black as an adult, [4] with larvae up to 1.25 inches (3.2 cm) long and adults up to 0.75 inches (1.9 cm) long. [5]

The yellow mealworm beetle can be differentiated from other beetles, due to the linear grooves that are evenly divided and run along the abdomen. The beetle has only four tarsal segments on its hind legs. Most ground beetles, which are similar in size to Tenebrio molitor, have five tarsal segments. [4]

Commonly mistaken with the black mealworm beetle ( T. obscurus ), key variations in regard to size and shape distinguish these two. The abdomen of the adult black mealworm beetle is more rounded and ends in a pointed tip, as opposed to the more rectangular and blunt-ended abdomen of the yellow mealworm beetle. [4] The larvae of T. molitor are lighter colored than those of T. obscurus. [5]

Distribution

Mealworms most-likely originated in the Mediterranean region, but are now present in many areas of the world as a result of human trade and colonization. The oldest archaeological records of mealworms can be traced to Bronze Age Turkey. Records from the British Isles and northern Europe are from a later date, and mealworms are conspicuously absent from archaeological finds from ancient Egypt. [6]

Life cycle

The eggs hatch 4 to 19 days after the female oviposits. [7]

During the larval stage, the mealworms feed on vegetation and dead insects, and molt between each larval stage, or instar (9 to 20 instars). After the final molt, they pupate. The new pupa is whitish and turns brown over time. After 3 to 30 days, depending on environmental conditions such as temperature, it emerges as an adult beetle. [7]

As larvae

In studies, T. molitor larvae show an incubation period of seven to eight days and a period of three to four days for the first instar. After the first instar, there is significant variation for the number of days in each instar period, though variation may be due to malnutrition or pathogens. Before emergence, most larvae typically go through 15 to 17 instars, with very few larvae going through the 19 to 20 instars. [8]

The body length of the larvae gradually increases with each successive instar, reaching maximum length at the 17th instar. The body length decreases beyond the 17th instar. Pupation occurs after the 14th instar, with most larvae showing total pupation between the 15th and 17th instars. Larvae are white in the first instar and gradually turn brown after the second instar. [8]

Effect of parental age and temperature

Offspring produced by older beetles have shorter larval stages than those produced by younger beetles. Larvae from the older beetles also show a rapid weight increase at an earlier age than those from young parents. At 25°C, the larval stage was shortened, the number of larval molts decreased, and the durations of adult life decreased when parental age increased, compared to the beetles at 30°C. [9] Another study found that at 20°, 25°, and 30°C, parental age does not have any effect on the duration of the egg stage, or the weights of the eggs.

However, the amount of hatched eggs decreased when parental age increased. When eggs were laid during the first two months after emergence, approximately 90% of the eggs hatched. When they were laid after four months, only about 50% hatched. [9] It was found that larvae from young parents grow at a slower rate, compared to larvae produced by the same parents, nine weeks earlier. At 30°C, there were no other effects of parental age on the larvae. At 20° and 25°C, the larvae from young parents required significantly more time to complete development, and had more molts compared to the larvae from the same parents after they had aged one more or longer. The duration of adult life decreased when parental age increased. [9]

Reproduction

Tenebrio molitor larvae eating an apple slice

A sex pheromone released by male mealworms has been identified. [10] Inbreeding reduces the attractiveness of sexual pheromone signaling by male mealworms. [2] Females are more attracted to the odors produced by outbred males than the odors produced by inbred males. The reduction of male signaling capability may be due to increased expression of homozygous deleterious recessive alleles, caused by inbreeding. [11]

The mealworm beetle breeds prolifically. Males insert sperm packets with their aedeagus. Within a few days, the female burrows into soft ground and lays eggs. Over her adult lifespan of about 6-12 months, a female will, on average, lay about 500 eggs. [7]

Mating

Researchers examined whether female beetles preferred males infected by the tapeworm Hymenolepis diminuta as mates, or noninfected males. Virgin females were found to spend more time near and copulated more often, with noninfected males in the experiment. Mating behavior was also found to be influenced by the mass of the male beetle. A larger male was preferred and mated with first compared to a smaller male mate. Overall, female beetles showed mating preferences for noninfected males who were larger in size. One explanation provided by researchers for this findings is that noninfected males who are larger may allow females to gain genetic or material benefits. [12]

Immunocompetence

Evidence suggests that in many animal species, secondary sexual traits reflect male immunocompetence, the ability of an individual’s immune system to resist and control pathogens or parasites. A study found that a single parasite-like immunological challenge, created via a nylon monofilament implant in the beetle, significantly reduced the sexual attractiveness and locomotor activity of males, it did not negatively affect their survival. When the inserts were removed, the majority of the males showed greater encapsulation responses of the implant, though some of the males seemed to have already chosen a terminal reproductive investment strategy. [13] And thus, the majority of males invest in their immune system after the first challenge.

A second immune challenge increased their attractiveness, but was found to significantly reduce locomotor activity of the males and increase their mortality. This represents a trade-off between pheromone production and energy required for activities such as immune system recovery and locomotor activity. [13]

When there was a third challenge, implantation, in the same males, there was a lower encapsulation rate of the nylon implants in more attractive males than the less attractive, showing how the males made no attempts to boost their immune system. [13] The results suggest that the males who become sexually attractive after the second immune challenge have a trade-off, where they sacrifice locomotor activity and do not energetically invest in immune system recovery. This shows how the female mealworm beetles consistently preferred males who invested significantly less in immune system recovery, and that males are not able to allocate resources simultaneously to both improving their health, or in this case, recovery of their immune system, and to increasing their sexual attractiveness. [13]

Nutritional condition

Pheromones are chemical signals that function as mate attractors and relay important information to prospective mates. For a reliable signal, it must be costly to produce, which means it is likely to have condition dependent expression. A study found that female preference of the pheromones was dependent on the nutritional condition of the males. They spent significantly more time with males who received constant food, than males who received no food. [14] Phenoloxidase activity was dependent on the nutritional condition of the males, with phenoloxidase activity being two to six times higher in males with constant food, than in males who received no food. However, nutritional conditions had no effect on the encapsulation rate of the males. [14]

When receiving constant food, male initial body mass had no correlations with phenoloxidase activity or encapsulation rate. This shows that pheromone mediated attractiveness and the immunocompetence in terms of phenoloxidase activity of males were condition-dependent, as both decreased with nutritional stress. This suggests that there is a trade-off between allocation of resources and energy into the production of pheromones and immunocompetence, and that the production of pheromones are condition dependent sexual traits. [14]

Immune defense

The mealworm beetle is currently considered a pest when infesting and degrading the quality of stored grains or grain products. However, they are now being promoted as a beneficial insect, as their high nutrient content makes them a viable food source for pet food, protein-rich animal feed, or even human nutrition, and they are capable of degrading plastic waste and polystyrene. [15] These benefits make mealworms attractive for mass rearing, a technique that promotes disease transmission within the colonies.T. molitor can be the host of many different pathogens and parasites, including entomopathogenic microbes, protozoa, and tapeworms, which can decrease the mealworm beetle’s survival or reproductive success. [15]

Behavioral immunity

When the mealworms feed on infected rodent feces, they may consume the eggs of the tapeworm parasite Hymenolepis diminuta . Infected male beetles pay a higher reproductive cost than the female beetles. T. molitor displays behavioral immunity when exposed to H. diminuta, shown by how the infected males develop an avoidance behavior for feces that harbor the tapeworm, which decreases their probability of coming into contact with the tapeworm in the future. [15] The female mealworm beetles develop a qualitative resistance through mate choice, as they are able to evaluate male immunocompetence through pheromone signaling, allowing them to choose the more immunologically fit males as mates. This also reduces the probability of the females being infected by their mates, and may cause them to pass on an enhanced level of immunocompetence to their offspring. [15]

Another way mealworms may display behavioral immunity is how they may tolerate infections by limiting negative effects on their reproductive success. For example, mealworm beetles tolerate a high number of cysticercoids of H. diminuta at the expense of their own fitness and longevity. But the males produce improved spermatophores that contain superior nuptial gifts that will be passed to their mating females, increasing female fecundity and causing a greater number of eggs to be fertilized. [15]

Cuticular color

Cuticular color, a heritable component, of the mealworm beetle varies from tan to black. In the mealworm beetle, evidence suggests that population level variation in cuticular color is linked to pathogen resistance in that darker individuals are more resistant to pathogens. A study found that two immune parameters related to resistance, haemocyte density and pre-immune challenge activity of phenoloxidase, were significantly higher in selection lines of black beetles compared to tan lines. Higher haemocyte density is likely indicative of a heightened immune response. [16]

There were no effects of gender on the immune traits. Cuticular color is dependent on melanin production, which requires phenoloxidase, an enzyme that is present in its inactive form inside haemocytes. This shows why darker insects have a heightened immune response and are more resistant to pathogens that invade the hemocoel via the cuticle. However, there was no significant difference in haemolymph antibacterial activity between black and tan lines, explained by how antimicrobial peptides are produced by haemocytes but are not involved in cuticular darkening. [16]

In T. molitor, the degree of cuticular melanization is a strong indicator of resistance to the entomopathogenic fungus Metarhizium anisopliae , which could be explained by the thicker and less porous cuticle displayed by darker insects compared to lighter ones. However, there seems to be underlying trade-offs that prevent the fixation of the darker phenotype, shown by how the plasticity of melanization phenotypes in response to population density may contribute to the absence of predominance of darker individuals among T. molitor populations. [15]

Food restriction

Because immune defenses against parasites and pathogens require metabolic resources, food restriction can impair immune function of T. molitor. For adult T. molitor beetles, phenoloxidase activity can be reduced by half during short-term food deprivation, but returns rapidly to original levels when the beetles are given access to food again. [15] T. molitor larvae can eat five times more food per day than usual following an immune challenge, to compensate for the caloric loss from the immune response. These immune challenged larvae show significant weight loss when fed with either protein or carbohydrate rich diets, but show stable weights when given both protein and carbohydrate-rich diets. [15]

Healthy T. molitor larvae usually prefer diets with a lower protein to carbohydrate ratio, but shift toward food with higher protein contents after an immune challenge with bacteria. This causes enhanced hemocyte circulation and antibacterial activity in the hemolymph, which likely maximizes resistance against bacterial infection. However, phenoloxidase activity is not affected by this shift in diet choice. [15]

A study found that the effects of nutritional imbalance on body composition were buffered by the subsequent selection of complementary foods. This demonstrates that the mealworm beetles are capable of compensating for nutritional imbalances and that the way nutritional balance is restored depends on the nutrient that is initially deficient in their food. [17] For example, if the beetles were previously fed a protein-rich, carbohydrate-deficient diet, they would prefer carbohydrates to protein, whereas beetles fed a carbohydrate-rich, protein-deficient diet, they would strongly prefer a protein-rich diet. They found that self-selecting T. molitor beetles recovered from carbohydrate or protein deficiency within six days by selecting the complementary diet. [17]

Gut microbiota

The gut microbiota of T. molitor consists of many different bacterial species present at low abundance. A study found a predominance of genus Spiroplasma species in the phylum Tenericutes in the gut samples of T. molitor, but there was variation found in the community composition between individuals. Although some Spiroplasma species are known insect pathogens, the T. molitor larvae did not experience any harmful effects from the presence of the Spiroplasma in the gut, indicating that they are not pathogens to the host. [18]

By comparing this to the bacterial communities found in other insects, it was found that the Spiroplasma species found were specific to T. molitor. The gut bacteria community structure was not significantly affected by the presence of antibiotics or by the exposure of the beetle larvae to a more highly diverse soil bacteria community. There is a negative relationship between bacterial diversity and ampicillin concentration, meaning ampicillin treatment caused a reduction in the bacterial community size, which was determined with pyrosequencing of the 16S rRNA gene, and no negative relationship when kanamycin was added. [18]

Polystyrene foam decreases T. molitor fecundity, but the beetle can fully develop using the plastic as its primary source of food, which makes it an interesting alternative to recycle polystyrene. However, when the mealworm’s microbiota is disrupted by an antibiotic treatment, it loses its ability to digest polystyrene, suggesting that its associated gut microbes are essential in the digestion process. Specifically, the bacterium Exiguobacterium species, which was isolated from the midgut of mealworms, was demonstrated to degrade polystyrene in vitro. [15]

Relationship with humans

As feed and pet food

Mealworms are typically used as a pet food for captive reptiles, fish, birds, and some small mammals. They are also provided to wild birds in bird feeders, particularly during the nesting season. Mealworms are useful for their high protein content. They are also used as fishing bait. [19]

They are commercially available in bulk and are typically available in containers with bran or oatmeal for food. Commercial growers incorporate a juvenile hormone into the feeding process to keep the mealworm in the larval stage and achieve an abnormal length of 2 cm or greater. [20]

As food

Mealworms in a bowl Mealworm 01 Pengo.jpg
Mealworms in a bowl

Mealworms are edible for humans, and processed into several insect food items available in food retail such as insect burgers. [21]

Due to their high protein and fat content, as well as consuming large amounts of fiber, they represent a good food source for humans. They are high in oleic acid, which may decrease low-density lipoprotein (LDL) and increase high-density lipoprotein (HDL) levels in the blood. [8]

Mealworms have historically been consumed in many Asian countries, particularly in Southeast Asia. There, they are commonly found in food markets and sold as street food alongside other edible insects. Baked or fried mealworms have been marketed as a healthy snack food in recent history, though the consumption of mealworms goes back centuries. [3]

In May 2017, mealworms were approved as food in Switzerland. [22] In June 2021, dried mealworms were authorized as novel food in the European Union, [23] after the European Food Safety Authority assessed the larvae as safe for human consumption. [24] [25]

Mealworm larvae contain significant nutrient content. [19] For every 100 grams of raw mealworm larvae, 206 kilocalories and anywhere from 14 to 25 grams of protein are contained. [26] Mealworm larvae contain levels of potassium, copper, sodium, selenium, iron and zinc that rival those of beef. Mealworms contain essential linoleic acids. They have a greater vitamin content by weight compared to beef, B12 not included. [26] [27]

Mealworms may be easily reared on fresh oats, wheat bran or grain, with sliced potato, carrots, or apple as a moisture source. The small amount of space required to raise mealworms has made them relevant for scalable industrialized mass production. [28]

Possible health risks

Some evidence suggests that T. molitor may pose a health risk, as humans and animals can consume the eggs and larvae of the beetle with grain-based food. Although they are usually either digested or are excreted with feces, sometimes, they are able to survive and live in the alimentary tract. The first cases of T. molitor larvae in human organs date back to the 19th century, where their presence was observed in the gastrointestinal tract, including the stomach and intestines. [29] There were other cases, such as a reported ulcer infestation of T. molitor in an AIDS patient and a concerned urinary canthariasis in a ten year old boy in Iran in 2019, which was the last reported human case of canthariasis caused by T. molitor. However, there are very few reported cases of live larvae in animals, and there are no reports of gastrointestinal canthariasis in farm animals. [29]

In waste disposal

In 2015, it was discovered that 100 mealworms can degrade polystyrene into usable organic matter at a rate of about 34–39 milligrams per day. No difference was found between mealworms fed only Styrofoam and the mealworms fed conventional foods, during the one-month duration of the experiment. [30] Microorganisms inside the mealworm's gut are responsible for degrading the polystyrene, with mealworms given the antibiotic gentamicin showing no signs of degradation. [31] Isolated colonies of the mealworm's gut microbes, however, have proven less efficient at degradation than the bacteria within the gut. [31]

See also

Related Research Articles

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References

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  14. 1 2 3 Rantala, Markus J.; Kortet, Raine; Kotiaho, Janne S.; Vainikka, Anssi; Suhonen, Jukka (2003). "Condition Dependence of Pheromones and Immune Function in the Grain Beetle Tenebrio molitor". Functional Ecology. 17 (4): 534–540. Bibcode:2003FuEco..17..534R. doi:10.1046/j.1365-2435.2003.00764.x. ISSN   0269-8463. JSTOR   3598991.
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  17. 1 2 Rho, Myung Suk; Pum LEE, Kwang (2015-04-02). "Nutrient-specific food selection buffers the effect of nutritional imbalance in the mealworm beetle, Tenebrio molitor (Coleoptera: Tenebrionidae)". European Journal of Entomology. 112 (2): 251–258. doi:10.14411/eje.2015.030.
  18. 1 2 Jung, Jaejoon; Heo, Aram; Park, Yong Woo; Kim, Ye Ji; Koh, Helium; Park, Wooden (2014-05-27). "Gut Microbiota of Tenebrio molitor and Their Response to Environmental Change" (PDF). Journal of Microbiology and Biotechnology. 24 (7): 888–897. doi:10.4014/jmb.1405.05016. PMID   24861345.
  19. 1 2 Ravzanaadii, Nergui; Kim, Seong-Hyun; Choi, Won-Ho; Hong, Seong-Jin; Kim, Nam-Jung (2012-09-30). "Nutritional Value of Mealworm, Tenebrio molitor as Food Source". International Journal of Industrial Entomology. 25 (1): 93–98. doi: 10.7852/ijie.2012.25.1.093 . ISSN   1598-3579.
  20. ↑ Finke, M.; Winn, D. (2004). "Insects and related arthropods: A nutritional primer for rehabilitators". Journal of Wildlife Rehabilitation. 27: 14–17.
  21. ↑ Ledsom, Alex (13 January 2021). "Insect Market To Explode: EU Gives Green Light To Eating Mealworm". Forbes.
  22. ↑ "Insects as food" (in German). Bundesamt für Lebensmittelsicherheit und Veterinärwesen. 2017-04-28.
  23. ↑ "Commission Implementing Regulation (EU) 2021/882 of 1 June 2021 authorising the placing on the market of dried Tenebrio molitor larva as a novel food under Regulation (EU) 2015/2283 of the European Parliament and of the Council, and amending Commission Implementing Regulation (EU) 2017/2470". EU Commission. 2 June 2021.
  24. ↑ Turck, Dominique; Castenmiller, Jacqueline; De Henauw, Stefaan; Hirsch-Ernst, Karen Ildico; Kearney, John; MacIuk, Alexandre; Mangelsdorf, Inge; McArdle, Harry J.; Naska, Androniki; Pelaez, Carmen; Pentieva, Kristina; Siani, Alfonso; Thies, Frank; Tsabouri, Sophia; Vinceti, Marco; Cubadda, Francesco; Frenzel, Thomas; Heinonen, Marina; Marchelli, Rosangela; Neuhäuser-Berthold, Monika; Poulsen, Morten; Prieto Maradona, Miguel; Schlatter, Josef Rudolf; Van Loveren, Henk; Ververis, Ermolaos; Knutsen, Helle Katrine; Knutsen, H. K. (13 January 2021). "Safety of dried yellow mealworm (Tenebrio molitor larva) as a novel food pursuant to Regulation (EU) 2015/2283]". EFSA Journal. 19 (1): 6343. doi:10.2903/j.efsa.2021.6343. PMC   7805300 . PMID   33488808.
  25. ↑ Boffey, Daniel (2021-01-13). "Yellow mealworm safe for humans to eat, says EU food safety agency". The Guardian. ISSN   0261-3077 . Retrieved 2021-01-15.
  26. 1 2 "6. nutritional value of insects for human consumption" (PDF). Edible insects: future prospects for food and feed security (PDF). FAO FORESTRY PAPER. Vol. 171. FAO. 2013. pp. 67–.
  27. ↑ Schmidt, Anatol; Call, Lisa; Macheiner, Lukas; Mayer, Helmut K. (2018). "Determination of vitamin B12 in four edible insect species by immunoaffinity and ultra-high performance liquid chromatography". Food Chemistry. 281: 124–129. doi:10.1016/j.foodchem.2018.12.039. PMID   30658738. S2CID   58651702.
  28. ↑ Rumbos, Christos I.; Athanassiou, Christos G. (March 2021). "Insects as Food and Feed: If You Can't Beat Them, Eat Them!'—To the Magnificent Seven and Beyond". Journal of Insect Science. 21 (2): 9. doi:10.1093/jisesa/ieab019. PMC   8023366 . PMID   33822126.
  29. 1 2 Gałęcki, Remigiusz; Michalski, Mirosław Mariusz; Wierzchosławski, Karol; Bakuła, Tadeusz (2020-11-11). "Gastric canthariasis caused by invasion of mealworm beetle larvae in weaned pigs in large-scale farming". BMC Veterinary Research. 16 (1): 439. doi: 10.1186/s12917-020-02657-0 . ISSN   1746-6148. PMC   7659124 . PMID   33176765.
  30. ↑ Jordan, Rob (29 September 2015). "Plastic-eating worms may offer solution to mounting waste, Stanford researchers discover". Stanford News Service. Archived from the original on 20 February 2021. Retrieved 24 March 2016.
  31. 1 2 Lockwood, Deirdre (September 30, 2015). "Mealworms Munch Polystyrene Foam". Chemical and Engineering News . Retrieved 2019-02-04.
  32. ↑ Madigral, Alexis C. (27 December 2012). "Who Was First in the Race to the Moon? The Tortoise". Atlantic. Retrieved 9 March 2019.
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