Minerals in edible insects: a review of content and potential for sustainable sourcing

Mingxing Lu,Chenxu Zhu,Sergiy Smetn*,Ming Zho,Hibo Zhng,Fng Zhng,Yuzhou Du,d,*

a College of Plant Protection &Institute of Applied Entomology,Yangzhou University,Yangzhou 225009,China

b German Institute of Food Technologies (DIL e.V.),Quakenbrück D-49610,Germany

c Jiangsu Plant Protection and Plant Quarantine Station,Nanjing 210036,China

d Joint International Research Laboratory of Agriculture and Agri-Product Safety,Yangzhou University,Yangzhou 225009,China

Keywords:Edible insects Minerals Nutrition Food safety Sustainability

ABSTRACT In response to the rapid increase in world population and subsequent demands for food,edible insects represent an alternative food source for humans that is rich in proteins,amino acids and minerals.Entomophagy is a tradition in many countries including China and Thailand,and edible insects have attracted a lot of attention in Western World due to their suitable nutrient composition,high mineral content (e.g.,Fe,Zn,Ca,Mg) and potential use as a supplement in human diet.In this study,we surveyed mineral content in seven insect orders and 67 species of mass produced and wild-harvested edible insects.The total content of essential elements in edible insects was very high in Tenebrio molitor,Bombyx mori,and Zonocerus variegatus.The heavy metal content (summarized for eight species) was below the maximum limit allowed for safe consumption.Sustainable supply of minerals derived from insect biomass is complicated due to the high variations of mineral content in insects and the potential of its change due to processing.

1. Introduction

Minerals are one of seven essential nutrient groups required for the human body and are used to form tissues and maintain normal physiological functions.Since minerals cannot be synthesized by the body,a daily intake is essential to support various physiological and biochemical processes[1].Minerals are generally divided into macro elements that are needed in large amounts (Ca,Mg,K,Na) and trace elements (Fe,Cu,Zn,Mn) that are needed in smaller quantities.From the perspective of food and safety,minerals are also categorized as essential elements (Ca,Mg,Fe,Zn,K) or nonessential elements (Hg,Pb,Cd) with respect to performing physiological functions in living organisms.The content of essential elements in the body is relatively stable,but unstable or low levels can disrupt bodily functions.Furthermore,excessive levels of some minerals can be toxic to the organism[2].Nonessential elements include heavy metals (Hg,Cr,Cd,As,Pb) that are toxic at high doses[3-4].Heavy metal pollution originates from industrial and automotive exhaust,agricultural pesticides and fertilizers,domestic garbage and sewage,medical waste and spoilage,and radioactive pollution.The sources of heavy metals may be hazardous to the environment,humans,plants,and animals.Plants and crops cultivated in contaminated soil often grow abnormally and may threaten food security and safety via pollution of the food chain.Insects,including edible species,may feed on water,plants and/or fruits that are contaminated,thus causing problems to humans that ingest them.

The world population is increasing at an alarming rate and is predicted to reach about 10 billion in 2050 when demands for food will rise by approximately 50%[5-6].Consequently,the development and use of alternative food sources is strongly encouraged due to increasing demand for animal protein and minerals;this is a global issue and includes food and feed insecurity,environmental pressures,wasteful disposal of food and resources,and unsustainable food production practices[7-10].Concurrently,the rapid pace of urbanization,industrialization,land-use changes,and pesticide usage has resulted in heavy metal pollution worldwide[11],which poses a threat to the environment and all life forms.

Edible insects such as the larvae of yellow mealworms and black soldier flies have great potential as alternative food/feed sources and possess high nutritive value due to their amino acid composition and mineral,vitamin,and polyunsaturated fatty acid content[9-10,12-13].Insects exhibit a higher fecundity and feed conversion efficiency than cattle,pigs,and poultry,and can transform low-value substrates into a high-value food resource[7,10,14].Furthermore,insect breeding is environmentally-friendly since insects need little space,minimal water,produce less greenhouse gas and emit less ammonia than conventional farm animals[15-18];these characteristics have important environmental,economic,and food security benefits.The consumption of insects or entomophagy is practiced in many parts of the world[19].In Asia and Africa,entomophagy is fairly common;for example,the consumption ofClanis bilineata tsingtauicaMell in China is over 300 years old.Insects are eaten raw or may be fried,boiled or processed in powder form as a food additive to enhance taste and aroma[20-22].In the Western World,edible insects such asTenebrio molitorandHermetia illucensL.are sometimes used to replace conventional sources of animal protein and represent a novel form of nutrition for both humans and animals in the food and feed industry[21,23-24].The large diversity in insects poses a challenge in implementing these species into the food and feed production chain[7,13].

There is a lot of knowledge available on the content and properties of macro elements in different insect species.The content,properties and accumulation of meso-and micro-elements,on the other hand is sporadic and not well systemized.The nutritional value of edible insects is highly variable and largely depends on their feeding substrates.Edible insects can obtain minerals such as Ca,Fe,Zn and Mg from feed or artificial diets;however,it is important to note that feeding substrates may also contain heavy metals,potentially available to insects[25].Insects can also accumulate heavy metals,dioxins and other hazardous compounds due to the breakdowns in harvesting and processing methods[10,26].Furthermore,heavy metals can accumulate in all life stages of insects and cannot be further degraded[26-27].The distribution and accumulation of other microelements is rather poorly presented and not systemized.Therefore,this review aims to summarize the information on the accumulation of essential meso-and microelements in edible insects and the main routes for the incorporation of minerals.

2. Methods

A systematic review was performed to define the scope of this topic concerning the content of minerals in edible insects and the potential of edible insects as sustainable and alternative sources.Three primary databases were searched,including Web of Science,ScienceDirect,and PubMed,on the deadline which was April 2022.The search terms used were: “insects”,“minerals”,“nutritional composition”,“edible insects”,“entomology”,“food safety”,and“heavy metals”.Then,a few specific criteria were set to select the appropriate sources for review,which include: studies should contain mineral category,content and accumulation pathways in edible insects,especially essential meso-and microelements,different dietary habits of edible insects in various regions,life cycle assessment of insects.A total of 89 bibliographic sources met the criteria and were considered in the review.

We compiled information on the essential mineral content in 67 edible insects belonging to one of the following seven orders:Coleoptera,Diptera,Hemiptera,Hymenoptera,Isoptera,Lepidoptera,and Orthoptera (Fig.1A).The number of edible insects summarized was highest in the order Orthoptera (22 species and subspecies),whereas the fewest number summarized was in Diptera (Drosophila melanogasterandMusca domestica) (Table 1).In these 67 species and subspecies,76.91% of the edible insects were wild-harvested,whereas reared edible insects accounted for 23.81% (Fig.1B).Furthermore,63.33% of the consumption consisted of the larval form of the surveyed insects (Fig.1C).

Fig.1 Representation of 67 edible insects by order,source and life stage.(A) Orders represented by 67 edible insects.Values inside the pie chart represent numbers in the same order.(B) Percentage of the 67 edible insects according to source (wild-harvested or reared).(C) Representation (%) of the 67 edible insects according to life stage consumed.

3. Essential and nonessential elements in insects

3.1 Essential mineral elements in edible insects

Edible insects are rich in nutritional value and are a potential source of minerals such as Cu,Fe,Mg,Mn,P,Se and Zn[28-29].The extent of mineral accumulation varies with the element,the species,and the growth phase of the insect[21];consequently,it is critical to understand the accumulation of essential minerals in edible insects to better utilize them in large-scale industrial production.

The essential element content was generally higher in larvae than adults,which may explain why larval forms are preferred over adults as food (Fig.1C).RearedT.molitorlarvae (Table 1) had the highest Ca,K,Mg,P,Na,Zn,Cu and Se level in the 67 insects summarized[30](Table 1).WildOnjiri mammonin Kenya exhibited the highest Fe levels at 1 562 mg/100 g[31](Table 1).WhereasSamia riciniipupae reared with castor had the highest Mn content at 254 mg/100 g[32](Table 2).RearedT.molitorlarvae that fed wheat bran and small amounts of carrots and potatoes had the highest mineral content at 335 105 mg/100 g[30](Table 1).

Table 2 The content of essential elements in S.ricinii and Z.variegatus at different life stages (mg/100 g of dry matter).

Prior research indicates that mineral content can vary according to insect life stage and diet.When 1st-3rdand 4th-6thinstar larvae ofZ.variegatuswere allowed to feed on leaves ofChromoelena odorataand cassava leaves,respectively,the different instars exhibited variable levels of essential minerals[33](Table 2).In another study,prepupae and pupae ofS.riciniifed on castor leaves contained different levels of Ca,Mg,P,Fe,Zn,Mn,and Cu;furthermore,S.riciniimineral levels varied between the food source;e.g.castor versus tapioca leaves[34](Table 2).Meanwhile,the essential mineral content ofS.riciniidiffers at different sexes and at different maturation stages.Female prepupae and pupae ofS.riciniitend to contain more mineral elements than male ones[32,34](Table 2).It is worth noticing that the mineral composition ofS.riciniidiffer largely between the report investigated by Ray and Gangopadhyay[34]

and Longvah et al.[32].This may be due to the geographical place of harvest,environmental factors and different processing methods[35].Insects originating in different countries or provinces also showed variability in essential element content,and examples included wildRhyncophorus phoenicislarvae from Angola and Nigeria[36-37],Polyrhachis vicinaRoger from Zhejiang,China and Guizhou,China[38]and semi-domesticatedVespa velutinalarvae and pupae from China and Korea[39](Table 3).Though harvested from the same place,the total mineral content of roastedRhyncophorus phoenicislarvae powder is higher than rawRhyncophorus phoenicislarvae[40](Table 3).Intraspecific variation in mineral content can also vary with insect color;for example,brown-and green-colored wildRuspolia differensshowed differences in Ca,K,Mg,P,Na,Fe,Zn,Mn,and Cu content[41].Differences in mineral content also varied between reared and wild edible insects of the same species;an example isS.gregariaadults where reared and wild individuals have different Ca,K,Mg,Na,Fe,Zn and Mn levels[41](Table 4).With respect to essential mineral content and recommended daily intake for adults,T.molitorlarvae,Zophobas morio,Oecophyllasp.,Anaphe venatalarvae,Conimbrasia belina,Acheta domesticusjuvenile crickets,and brownR.differensare highly nutritious edible insects for human consumption.

3.2 Nonessential mineral elements in edible insects

Insects may inadvertently ingest nonessential metals from food chains;for example,diets may be rich in heavy metals or metals may be assimilated through the exoskeleton or other surfaces via exposure[42].Some insect taxa are more likely than others to accumulate metals,whereas insects in Coleoptera have less contact with metals[43].

The levels of selected elements in insects are dependent on food source,species and breeding environment.For example,the content of Cu and Zn inT.molitorwas higher when fed with wheat bran than oat bran[13,28].After eating feed containing Ni,Zn and Pb,the increased heavy metal content in theSpodoptera lituramidgut,fat body,epidermis and hemolymph correlated with rising heavy metal concentrations in feed.The concentration of Cd in theOxya chinensisdigestive canal was higher than in other organs after feeding on wheat grown in Cd-contaminated soil.The content of Al,Cu,Ni,Zn and Cd inLymantria dispalarvae harvested from polluted areas are highest in the head as compared to other body parts.In China,heavy metal contamination in insects is a growing concern,and Cd,Pb and Hg have been reported in orders Diptera,Lepidoptera,Coleoptera,Hemiptera,and Orthoptera[42].The content of Hg inCryptotympana atrataharvested from Liaoning Province,China,was highest in the body followed by membranous wings;the exuvium has the lowest Hg concentration[42,44].

Table 5 provides a summary of nonessential heavy metal content in five species of edible insects from orders Coleoptera,Lepidoptera and Orthoptera.The content of As,Cd,Pb,Hg in wild or rearedHolotrichiasp.,T.molitor,Z.morio,B.mori,Patanga succincta,A.domesticus,Locusta migratoria,andSchistocerca gregariawere below the recommended limits in feed,which make these insects safe for consumption[45-46].It should be noted that potential heavy metal hazards could still exist in edible insects.Furthermore,even when heavy metal concentrations are all below the recommended limit,the accumulation of metals from numerous edible insects warrants attention and further research.

4. The sources and transformation pathways of minerals in edible insects

Insects cannot biosynthesize minerals but instead obtain essential and nonessential elements from exogenous sources[47],which can result in adverse effects on insect development and production[13,48].Insects obtain essential elements from water,soil,integument,and food sources including artificial diets (Fig.2).The bioavailability of minerals in edible insects varies with rearing methods,food matrix,the gastrointestinal digestive process,absorption and various metabolic process that regulate the transportation of nutrients to various organs[49].For example,the solubility of Fe is highest in crickets,and higher in mealworms than grasshoppers.The solubility of Cu,Mn,Ca,Mg and Zn were relatively high in crickets,mealworms and grasshoppers[50].

Fig.2 The sources and transmission pathways of minerals in insects.Question marks represent unknown conversion rates of metals from insects to feces,predators and next generation.

Both wild-harvested and farm-raised edible insects are vulnerable to the accumulation of micro-elements,known as heavy metals from feed and water.Wild-harvested insects have been shown to accumulate heavy metals including Hg,As and Pb[51].The uptake of mineral elements is not strongly regulated in insects.After uptake by insects,heavy metals can bind to metallothioneins or be sequestered in vesicles,which effectively negates their toxicity[13].In some cases,these elements are excreted into the lumen of the digestive tract via exocytosis.The yellow mealworm,T.molitor,was found to have two pools of Cd;a small proportion of Cd penetrated the epithelium through Ca2+channels to reach other issues,whereas the majority Cd was stored in the intestinal epithelium where it was bound by a Cd-binding protein[52-53].The midgut epithelial cells ofT.molitorhad a lifespan of four days,after which bound Cd was released into the lumen of the intestine and subsequently excreted in the feces[52].

When consumed in excess,metals can have various effects on invertebrate health,including a reduced immune response,prolonged development,and loss of mass;however,many invertebrates have evolved metal tolerance or detoxification mechanisms[27].Some invertebrates limit uptakes of metals and others excrete metals in their feces (Fig.2),thus reducing metal transfer to higher trophic levels.In some cases,metals can retain inside invertebrates.Relatively few studies investigate the conversion rate of metals from insects to the environment or their vertical accumulation through passing to the next generations.Different orders of insect show different conversion rates as well.Behavioral responses may limit the accumulation of metals in invertebrate tissues,even when in direct contact with metals.After the initial taste of a metal-rich plant,herbivorous invertebrates may develop an aversion and reduce ingestion rates[27].Some insects may avoid contaminated areas,especially during oviposition;for example,D.melanogasterandPlutella xylostellafemales avoid laying eggs on metal-rich plant materials.

It is well-established that a lack of essential elements such as Zn and Fe in the diet can impair human health.Although edible insects may help address food shortages and provide various nutrients,they are also at risk of exposure to heavy metals.

Although many insects are rich in minerals,only a few studies address their utilization and transformation alongside with other nutrients in edible insects during processing.Different life stages,sexes,feeding substrates and environmental conditions can impact mineral content in insects;thus,it is vital to determine best practices for rearing insects as food.Processing often involves harvesting,pre-processing,removing contaminates,packaging,and storing,and these steps can change mineral content and cause nutrient loss[20].The packaging of edible whole insects (dried,frozen,pre-cooked),the processing of extracts,and cooking methods (steaming,roasting,smoking,frying,stewing) can also alter or reduce mineral content[54].The processing of edible insects can lower the concentration of hazardous chemicals and reduce microbial load in the insect,which is higher in fresh insects than in processed forms[55].According to Ojha et al.[54],processing methods can contribute to the loss of nutrients and minerals.WhenEulepida mashonaandHenicus whellaniwere prepared by boiling,the bioavailability of Zn and Fe was significantly reduced[56];however,preparation by roasting did not reduce the availability of these two minerals[50].In the mopane caterpillar,Gonimbrasia belina,Ca availability increased after 5-7 min of roasting[57].

In this review,the content of heavy metals in eight different edible insects was below the recommended limit (Table 5);however,these species were reared artificially and did not include wild-harvested insects.Not onlyT.molitorlarvae can accumulate several heavy metals,which is a potential risk to food and feed safety.It is important to determine whether the metals present in insects gets accumulated and stored in human tissues after consumption.These questions circle back to the need to strengthen the regulation of edible insect sources,processing methods and safety[58].Although insects are short-lived and their accumulation of microelements might be considered as lower as compared to cows,sheep and chicken,it still should be better studied and monitored.

5. Sustainability approaches to the assessment of insectderived minerals use for food and feed

Insects are considered as a potentially sustainable source of proteins[59-60],lipids[61-63],and some specific bioactive compounds[64-65].Supply of minerals from insects has not been assessed from sustainability perspective,neither with Life Cycle Assessment (LCA)nor with other social or economic analyses.It is necessary to mention that there are only a few studies dealing with the sustainability assessment of mineral and additive supplies originating from other sources and used for feed formulations mostly[66-68].Those studies indicate relatively high environmental impacts,but the positive influence of supplements for health of animals.

It is necessary to point out that the supply of minerals is envisioned as a part of insect biomass to be consumed either as feed for animals or as food.In such approach supply of minerals should be viewed from the position of a complex nutrient supply.Therefore,the relative comparative sustainability assessment should be performed for complex foods,involving various amounts of nutrients and minerals[69-70].Moreover,sustainability assessment is directly related to the potential impact on the health of animals or humans,which calls for the need of diet-based assessment[71].

Indicated approaches to the sustainability assessment of minerals derived from insect biomass highlight the current trends in their assessment through the inclusion in the complex food matrices and therefore diets.Such approaches avoid the need to assess separate elements but get complicated due to the need to create nutrient indices,able to capture the complexity of nutritional profiles and dietary trends.

6. Future prospects

Further research is needed to identify methods that help retain optimal nutrient levels in edible insects.Additional studies are also crucial to understanding the chemical form of these essential elements in insects and whether people can absorb and utilize them.In this respect,edible insects have a promising future;with further technological improvement and innovation,the industry could move towards automation in large scale rearing and processing facilities.Edible insects could be processed into powders or other formulations and added to food ingredients to improve nutritional value.It will also be important to establish formal regulatory processes for the marketing and production of edible insects and their use as supplements.

Current research on mineral elements while focusing on heavy metals,especially on individual metals,does not present well insights on the combined stress of multiple heavy metals,neither their interaction with other nutrients (synergetic or antagonistic).It is also important to investigate whether meso-and micro-elements(including heavy metals) can be passed on to the next generation and what changes occur in progeny.Answers to these questions are critical for edible insects,which represent a new type of food that has the potential to improve human health.The early resolution of these issues will bring benefits and convenience to the production and promotion of insect food and make it more acceptable and safer for consumption.Moreover,the assessment of potential synergetic or antagonistic effects is needed for the supply of minerals from insect biomass with accounting of dietary and regional variations.

Acknowledgements

This research was founded by Jiangsu Agricultural Science and Technology Innovation Fund (CX (20) 3179),and Dongminghuanghetan Ecological Agriculture Co.,Ltd (204032897).This research is also partially funded funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement no.861 976,project SUSINCHAIN;and from the German Federal Ministry of Education and Research (BMBF),in the frame of FACCE-SURPLUS/FACCE-JPI project UpWaste,grant number 031B0934A.

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.