Journal of Insect Science, (2021) 21(2): 13; 1–11

doi: 10.1093/jisesa/ieab014
Review

The Superworm, Zophobas morio (Coleoptera:Tenebrionidae):

A ‘Sleeping Giant’ in Nutrient Sources
C. I. Rumbos1, and C. G. Athanassiou
Laboratory of Entomology and Agricultural Zoology, Department of Agriculture, Crop Production and Rural Environment, University
of Thessaly, Volos, Greece, and 1Corresponding author, e-mail: crumbos@uth.gr

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Subject Editor: Phyllis Weintraub

Received 22 December 2020; Editorial decision 3 February 2021

Abstract
The aim of this review is to compile up-to-date information on the superworm, Zophobas morio (F.), regarding
its biology and ecology, but also its further potential for use as a nutrient source for food and feed. We illustrate
certain basic characteristics of the morphology and bio-ecology of this species, which is marginally considered
as a ‘pest’ in durable amylaceous commodities. More recent data show that Z. morio can be a valuable nutrient
and antimicrobial source that could be utilized further in insect-based feed and food production. The inclusion of
this species in aquafeed has provided promising results in a wide range of feeding trials, both in terms of fish
development and health. Additional data illustrate its potential for use in poultry, indicating that this species provides
comparable results with those of other insect species that are used in feed. Moreover, Z. morio can be a viable waste
management agent. This review aims to summarize the available data and underline data gaps for future research,
toward the potential of the utilization of Z. morio for human food and animal feed. Based on the data presented,
Z. morio appears to be a well-promising insect-based protein source, which potential still remains to be unfold.

Key words: alternative nutrient source, insect farming, nutritional value, sustainability, Tenebrionidae

In a steadily increasing world population that is projected to get near 2013) efficient feed converters (Oonincx et al. 2015, Halloran et al.
to 10 billion by 2050, the demand for animal protein will continue 2016), they can be easily reared on organic side-streams and agricul-
to grow over the years to come (Boland et al. 2013, Searchinger tural wastes being aligned with circular economy strategies (Gasco
et al. 2018, FAO 2019). Indicatively, the per capita meat consump- et al. 2020), whereas their production has a low environmental foot-
tion is expected to increase >1 kg retail weight equivalent by 2027 print (Van Huis and Oonincx 2017). Apart from the aforementioned
at a global level (OECD-FAO 2018), while this increase will be more advantages, several species have specific physiological traits, such as
vigorous in developing countries where the per capita consumption high reproduction rate, short life cycle, rapid growth, as well as ease
of animal protein will rise by 22% by 2030 and 25% by 2050 (FAO/ in handling and manipulation, which favor their commercialization.
WHO 2017). However, the capabilities to increase animal protein Currently, a number of insect species are commercially produced in
production through the further intensification of the traditional large-scale industrial facilities (Van Huis 2019). Although insect con-
livestock production systems are rather marginal, as this would sumption is still not common in the western society, the increasing
trade-off with adverse environmental impacts, i.e., effect on climate willingness to adopt insect-based foods has been recently detected
change through greenhouse gas emissions, extensive land use for in several western countries (Schlup and Brunner 2018, Orsi et al.
livestock farming and deforestation, as well as extensive water usage 2019). Moreover, the majority of the population seems to not mind
and pollution (Steinfeld et al. 2006). Additionally, the animal feed consuming meat products originating from livestock that were fed
industry is seeking for new protein sources to reduce the dependence by insects (Kulma et al. 2020a). Therefore, new EU regulations have
and reliance of livestock production on soybean meal and fishmeal, been released in order to pave the way for these products. According
which are the main ingredients for animal feed. Therefore, there is to the EU Regulation 2017/893, in force since July 2017, seven insect
an urgent need for alternative animal proteins both for human con- species are so far allowed to be used in EU as ingredient in aquafeeds
sumption and feed production. [Commission Regulation (EU) 2017/893]. Regarding the production
Several insect species have been identified during the last decade as and consumption of insects as food in EU level, the ‘Novel Food’
an alternative protein source to be included in human food and animal legislation [Commission Regulation (EU) 2015/2283] regulates also
feed as they have numerous advantages (Van Huis 2013, Gasco et al. the dietary inclusion of insects in human diets, whereas more re-
2019). Namely, they are highly nutritious (Rumpold and Schlüter cently the approval of larvae of the yellow mealworm, Tenebrio

© The Author(s) 2021. Published by Oxford University Press on behalf of Entomological Society of America.
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2 Journal of Insect Science, 2021, Vol. 21, No. 2

molitor L. (Coleoptera: Tenebrionidae), for human consumption by

the European Food Safety Authority (EFSA 2021) is expected to be
a breakthrough in the promotion of insect-derived food products.
Among the most common mass-reared insect species, the black sol-
dier fly, Hermetia illucens (L.) (Diptera: Stratiomyidae) (Tomberlin and
Van Huis 2020), T. molitor (Ribeiro et al. 2018), and the lesser meal-
worm, Alphitobius diaperinus (Panzer) (Coleoptera: Tenebrionidae)
(Rumbos et al. 2019), have attracted most of the scientific and com-
mercial interest. However, the list of insects which have shown
potential for exploitation as a nutrient source and merit further in-
vestigation is extensive. One insect species with great potential as
food and feed, which has been overlooked by researchers and insect
producers is the superworm or giant mealworm, Zophobas morio (F.,
1776) (Coleoptera: Tenebrionidae). It is a large neotropical beetle spe-

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Fig. 1. Number of published articles per annum indexed by Google Scholar
cies, belonging to the darkling beetles family, which is commonly reared matching the search queries ‘Zophobas morio’ (bars, left axis) and ‘insect’
as feed for birds, reptiles and fish. Zophobas species are reported by (line, right axis), shown per year of publication (2000–2020) (Date of Google
Ramos-Elorduy (2009) to be eaten by several ethnic groups in Mexico, Scholar search: 27 January 2020).
whereas Z. morio is reported as one of the two main insect species,
together with the field cricket, Gryllus assimilis (F.) (Orthoptera:
nowadays been also introduced to other regions in Europe and Asia
Gryllidae), bred in captivity in Brazil, intended only for animal feed
(Yuan et al. 2012, Fursov and Cherney 2018).
(Araújo et al. 2019). The first research records on Z. morio date back
to the 1970s and 1980s (Tschinkel and Willson 1971; Tschinkel and
van Belle 1976; Tschinkel, 1978, 1981, 1993). However, since then Identification, Key Characteristics, and Biology
a considerable amount of research on Z. morio has been conducted
(Kim et al. 2015, Van Broekhoven 2015, Van Broekhoven et al. 2015, Eggs
Harsányi et al. 2020). Indicatively, the number of research articles on The eggs of Z. morio are oval with rounded edges, white and ~1.7 mm
Z. morio published each year has exponentially increased during the in length and 0.7 mm in width (Fig. 2A; Fursov and Cherney 2018).
last decade (Fig. 1), with the main focus of the recent studies being the Each female can lay a high number of eggs (up to 2,200) during its life-
potential of Z. morio as a nutrient source for livestock animal feed and span, with the number of eggs being negatively correlated with female
aquaculture. Recently, the complete mitochondrial genome of Z. morio maternal age and positively correlated with adult density (Tschinkel
was sequenced (Bai et al. 2019), signifying the increased interest of 1993).
researchers for this species. In this framework, this review aimed to
present collectively significant information on Z. morio, in order to Larvae
better highlight its potential as a nutrient source for food and feed The larvae are yellow with dark brown anterior and posterior
and provide a useful tool for researchers working with this promising ends (Fig. 2B; Fursov and Cherney 2018). They have a cylindrical,
beetle species. strongly sclerotized exoskeleton, conically narrowed from the base
of the seventh to the ninth abdominal segment. They can get up to
55-mm long (Friederich and Volland 2004). They hatch after 8 d
at 25°C (Kim et al. 2015). The number and duration of larval in-
Taxonomy, Systematic Position, and
stars is density-dependent, i.e., it varies depending on whether larvae
Distribution are maintained under isolated or grouped conditions. For instance,
The taxonomy and classification of Z. morio [formerly Tenebrio the isolation of newly hatched larvae considerably prolongs their
morio (F., 1778); Helops morio (F., 1777)] has been a matter of development time in comparison to early instar larvae kept under
controversy and confusion (Tschinkel 1984; Ferrer 2006, 2011). grouped conditions (Quennedey et al. 1995). If kept isolated, larvae
Currently, Z. morio is identified as conspecific with Zophobas atratus pupate after 11–18 instars, whereas the largest percentage of pu-
(F., 1775) [formerly Tenebrio atratus (F., 1775); Zophobas rugipes pation occurs after 16 or 17 molts (Quennedey et al. 1995, Kim
(Kirsch, 1866) (Park et al. 2013, Soldati and Touroult 2014, Bousquet et al. 2015). One of the most interesting characteristics of this spe-
et al. 2018) and as such they will be considered in this review. cies is that its larvae fail to pupate under crowded conditions, al-
Zophobas morio belongs to the large beetle family of though larval molts continue to occur until death (Tschinkel and
Tenebrionidae, which contains many stored-product insect spe- Willson 1971, Quennedey et al. 1995). For instance, Tschinkel and
cies, such as T. molitor and A. diaperinus, but also the confused Willson (1971) demonstrated that the rate of pupation was retarded
flour beetle, Tribolium confusum Jacquelin du Val (Coleoptera: with the increase of larval density. This phenomenon does not seem
Tenebrionidae), and the red flour beetle, Tribolium castaneum to be pheromone-mediated, or to be caused by auditory or visual
(Herbst) (Coleoptera: Tenebrionidae). Although listed among storage stimuli and is rather attributed to the mechanical stimulation re-
insects, Z. morio has been found in association with only one stored sulting from inter-larval contacts (Tschinkel and Willson 1971). In
commodity, i.e., wheat flour (Hagstrum and Subramanyam 2009), terms of commercial production, the larval requirement for isolated
indicating its negligible importance as secondary storage insect pest. conditions for pupation, can significantly affect the industrialization
In nature, it has been reported in association with fruit bat guano of Z. morio production and impact its commercial production ef-
and organic litter (Tschinkel and Willson 1971). It traces its origins in ficiency. Pupation inhibition induced by crowding conditions has
the tropical regions of Central and South America (Marcuzzi 1984, been described also for other tenebrionid species, e.g., Tribolium
Tschinkel 1984, Hagstrum and Subramanyam 2009); however, it has freemani Hinton (Coleoptera: Tenebrionidae) (Nakakita 1982,
Journal of Insect Science, 2021, Vol. 21, No. 2 3

Kotaki et al. 1993) and has been proposed to be a defense mech- faster from small pupae) and temperature (faster adult eclosion at
anism against cannibalism that is often observed among larvae and 29°C) (Quennedey et al. 1995). Similarly to other tenebrionid spe-
pupae (Tschinkel and Willson 1971, Ichikawa and Kurauchi 2009). cies, such as T. molitor (Bhattacharya et al. 1970) and A. diaperinus
It is suggested that different hormones, such as ecdysteroids and ju- (Esquivel et al. 2012), individuals can easily be sexed at this life stage
venile hormones, play a role in this larval developmental variability by noting two distinct projecting pygopods at the ninth abdominal
(Quennedey et al. 1995, Aribi et al. 1997). Approximately 6 d after segment of the female pupae close to the urogomphus, which are ab-
isolation at 25°C, larvae get immobilized as prepupa in a c-shaped sent from the male ones (Fursov and Cherney 2018).
posture, which marks the initiation of the metamorphosis process.
The prepupae do not walk, but respond to tactile stimuli by flicking Adults
their body, whereas it takes them seven more days to become pupae They are large (38- to 57-mm body length) with elongated body and
(Quennedey et al. 1995). filiform antennae (Fig. 2D). The surface of the elytra is punctuated
with nine rows of bristle-bearing punctures. Adults can live up to 6
Pupa mo (Fursov and Cherney 2018).

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The pupae (Fig. 2C) are mostly quiescent, however, when tactile
stimulated, they have the ability to rotate their abdominal segments
in a circular motion (Ichikawa and Kurauchi 2009, Ichikawa et al. Rearing
2012b) or exhibit other physical responses (Ichikawa et al. 2012a, Information on the dietary requirements of Z. morio is available
Ichikawa and Sakamoto 2013). All these reactions are considered to in several studies. Larvae are commonly produced on wheat bran
be an effective pupal defense mechanism against predator attacks alone (Quennedey et al. 1995, Aribi et al. 1997) or supplemented
and larval cannibalistic behaviors and are triggered by the stimu- with various cereal grains (e.g., oat) or other related amylaceous
lation of different types of mechanoreceptive sensilla on the pupal commodities (Maciel-Vergara et al. 2018). A moisture source, e.g.,
body surface (Kurauchi et al. 2011). The duration of the pupal stage fruit peelings (Quennedey et al. 1995), carrots (Van Broekhoven
is 13–15 d at 25°C, depending on the pupal weight (adults emerging et al. 2015), or other organic materials with high water content, is

Fig. 2. Life stages of the superworm, Zophobas morio, from egg to adult: (A) eggs, (B) late-instar larva, (C) pupa, and (D) adult.
4 Journal of Insect Science, 2021, Vol. 21, No. 2

provided to larvae and adults in order to cover their water needs, ranges between 6.2 and 8.6% (Table 1), whereas it is not affected by
as larvae deprived of water exhibit strong cannibalistic behavior their age (Kulma et al. 2020b). Not surprisingly, a higher total nitrogen
(Ichikawa and Kurauchi 2009). Lately, there has been an increasing content (10.8%) was estimated for defatted flour from Z. morio larvae
interest in the valorization of organic side-streams for the rearing (Botella-Martínez et al. 2020). We avoid intentionally in this review to
of Z. morio (Van Broekhoven 2015, Van Broekhoven et al. 2015, refer to protein content, since no protein-to-nitrogen conversion factor
Harsányi et al. 2020). For instance, Van Broekhoven et al. (2015) (Kp) has been proposed for Z. morio individuals, as is the case for other
reported that Z. morio larvae could grow successfully on most diets related species, such as T. molitor and A. diaperinus (Janssen et al. 2017,
tested composed of spent grains and beer yeast, bread and cookie Boulos et al. 2020). Therefore, the Jones’ default nitrogen-to-protein
remains, potato steam peelings, and maize distillers’ dried grains. In conversion factor of 6.25 that all studies have used so far to convert
contrast, the dietary inclusion of vegetable and garden waste, as well nitrogen content to protein may overestimates the body protein content
as of cattle and horse manure resulted to reduced growth compared due to the chitin nitrogen of Z. morio individuals. For larvae, the chitin
with chicken feed used as control diet (Harsányi et al. 2020). content has been reported to be 3.9–6% (Adámková et al. 2017, Soon
Regarding rearing conditions, temperatures ranging between 25 et al. 2018, Shin et al. 2019, Benzertiha et al. 2020, Kulma et al. 2020b).
and 28°C and an average relative humidity of 60–70% are com- A full physicochemical characterization of chitin, as well as its derivative

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monly used for Z. morio production. Although high growth rates chitosan, from Z. morio larvae is provided by Soon et al. (2018). The
have been reported for Z. morio larvae (Zaelor and Kitthawee amino acid profile of Z. morio larvae contains relatively high amounts
2018), these are reduced under crowding conditions (VandenBrooks of all essential amino acids, with the exception of methionine (Table 2).
et al. 2020). Cannibalism occurs often in Z. morio (Tschinkel Regarding fat content, Z. morio larvae have a high proportion of lipids,
1981, Ichikawa and Kurauchi 2009), negatively affecting biomass ranging between 35.0 and 43.6% (Table 1), considerably higher that
production and yield, although it does not appear to be density- other insect species also considered as nutrient source (Barroso et al.
dependent (Zaelor and Kitthawee 2018). Moreover, when talking 2014). According to their fatty acid profile, Z. morio larvae have high
about commercial large-scale production, care should be taken to saturated fatty acid (SFA) and monounsaturated fatty acid (MUFA)
avoid disease outbreaks that could totally devastate the insect cul- content, with palmitic and oleic acid being the most abundant ones,
tures. Information about diseases of this species is limited, however, respectively (Table 3). Among polyunsaturated fatty acids (PUFA), the
there are few reports that start providing insight into the occurrence omega-6 linoleic acid is abundantly found in Z. morio larvae (Table 3;
of infectious microbial agents of Z. morio (Liu et al. 2012, Bakonyi Barroso et al. 2014). Apart from their high nitrogen and lipid content,
et al. 2015, Maciel-Vergara et al. 2018, Tokarev et al. 2019). The Z. morio larvae contain several minerals (Table 4), as well as vitamins
cannibalistic behavior of Z. morio larvae seems to further enhance (Finke 2002, 2015).
the transmission of microbial agents, offering additional entry routes In contrast to larvae, only one study has investigated the nu-
to pathogens (Maciel-Vergara et al. 2018). Regarding mass produc- trient profile of Z. morio adults (Oonincx and Dierenfeld 2012).
tion methods for Z. morio, available information on the efficient, Compared with larvae, adults have a higher nitrogen content
cost-effective and sustainable large-scale production of this species is (10.9%), which could be attributed mainly to the higher propor-
rather limited, in contrast to other insect species, such as T. molitor tion of chitin of the well-sclerotized adults (Finke 2007); however,
and H. illucens, whose industrial production has attracted already no information is available so far on the chitin content of adults. In
considerable attention. Still, these methods are not expected to be contrast, adult fat content is considerably lower (14.3%) in com-
sufficiently different than those that are currently in use for the rela- parison to larvae, following the general trend according to which
tive T. molitor. larvae are more rich in fat than adults (Kouřimská and Adámková
2016). The limited interest on the exploitation of Z. morio adults
as nutrient source may be attributed to specific traits of these bee-
Nutritional Value tles that render their consumption unfavorable. For instance, simi-
Studies of the nutritional profile of Z. morio larvae have shown its high larly to other tenebrionid beetles such as T. molitor (Attygalle et al.
nutritional value (Barker et al. 1998; Finke 2002, 2007, 2015; Barroso 1991), Z. morio adults produce, as a chemical defense mechanism,
et al. 2014; Bosch et al. 2014; Adámková et al. 2016, 2017; Araújo various volatile secretions through their abdominal glands, mainly
et al. 2019). Larvae are rich in nitrogen, as their total nitrogen content quinones (Tschinkel 1969, Hill and Tschinkel 1985), which have
an undesirable odor and taste (Belluco et al. 2013). Additionally,
time-to-harvest is more increased for adult beetles compared with
Table 1. Proximate composition of Zophobas morio larvae and larvae, requiring more feed, energy and space to rear them up to
adults

Larvaea Adultsb
Table 2. Amino acid content (% DM) of Zophobas morio larvae
Dry matter (% as fed) 35.2–42.1 38.2
Total nitrogen (% DM) 6.2–8.6 10.9 Arginine 2.2–3.5 Valine 2.4–3.4
Crude fat (% DM) 35.0–43.6 14.3 Histidine 1.4–2.3 Alanine 3.4–4.0
Ash (% DM) 2.4–8.2 6.2 Leucine 3.4–4.5 Aspartic acid 3.8–4.7
Neutral detergent fiber (NDF) (% DM) 9.3–13.0 50.1 Lysine 2.4–2.9 Glycine 2.3–3.0
Acid detergent fiber (ADF) (% DM) 6.3–6.5 32.1 Isoleucine 2.2–2.4 Serine 2.2–2.7
Energy (kcal/100 g DM) 559.2–575.5 n.r. Phenylalanine 1.6–2.2 Proline 2.6–3.7
Methionine 0.5–1.0 Cystine 0.4–0.5
(n.r.) not reported Threonine 1.9–2.0 Glutamic acid 5.7–6.6
a
Values show the range of mean values from published sources (Barker Tryptophan 0.4–0.5 Tyrosine 3.3–3.9
et al. 1998; Finke 2002, 2007, 2015; Yi et al. 2013; Barroso et al. 2014; Bosch
et al. 2014; Adámková et al. 2016, 2017; Araújo et al. 2019). Values show the range of mean values from published sources (Finke 2002,
b
Source: Oonincx and Dierenfeld (2012). 2007, 2015; Bosch et al. 2014).
Journal of Insect Science, 2021, Vol. 21, No. 2 5

Table 3. Fatty acid composition (% DM and % of total fatty acids) of fishmeal with Z. morio meal in fish feeding trials (Table 5),
of Zophobas morio larvae as its nutrient profile easily meets the basic fish nutrient require-
ments. Particularly, apart from being a high protein source, Z. morio
Fatty acid % DM % of Total fatty acids
meal contains adequate quantities of the most limiting amino acids
Palmitic (C16:0) 9.7–12.5 29.1–32.4 in fish diets, i.e., lysine, threonine, and arginine, with the exception
Palmitoleic (C16:1) 0.2–0.4 1.0–3.2 of methionine, in which it is deficient (Table 2). In a recent study,
Stearic (C18:0) 3.0–3.1 6.4–8.8 15 and 30% dietary inclusion of full-fat Z. morio larvae meal in
Oleic (C18:1) 11.6–15.7 31.1–38.0 replacement of soybean meal and soybean oil did not impact the
Linoleic (C18:2) 7.1–7.8 15.6–23.4 survival and growth performance of Nile tilapia [(Oreochromis
Saturated (SFA) – 38.8–44.6
niloticus (L.)] juveniles (Alves et al. 2020). However, in the same
Monounsaturated (MUFA) – 32.1–42.4
study, the fish body composition was altered by insect meal inclusion,
Polyunsaturated (PUFA) – 15.7–24.0
Omega-6 – 16.5–24.0
as fish fed on the diets containing 30% Z. morio meal had higher
moisture and lipid contents and lower ash and protein contents, as
compared with fish that were fed on the control diet. Moreover, the

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Values show the range of mean values from published sources (Finke 2002,
2015; Barroso et al. 2014; Adámková et al. 2016, 2017; Kierończyk et al. inclusion of Z. morio in aquafeeds may positively influence several
2018; Araújo et al. 2019). innate immunity parameters (Alves et al. 2020). Regarding the di-
gestibility of Z. morio meal, Fontes et al. (2019) assessed the nu-
trient and energy apparent digestibility coefficients (ADCs) from
Table 4. Mineral composition (mg/100g DM) of Zophobas morio a Z. morio-based diet at a 20% inclusion level for Nile tilapia.
larvae and adults According to their findings, the Z. morio meal-based diet, together
Mineral LarvaeA Adultsb with the T. molitor meal-based diets, showed higher ADCs for en-
ergy and dry matter compared with the other diets tested containing
Calcium 31.9–70.8 60.0 insect meals of the speckled cockroach, Nauphoeta cinerea (Olivier)
Phosphorus 562.9–564.9 710.0 (Blattoidea: Blaberidae), the hissing cockroach, Gromphadorhina
Magnesium 39.2–118.3 150.0 portentosa (Schaum) (Blattodea: Blaberidae), and G. assimilis.
Sodium 104.1–112.8 180.0
Specifically, T. molitor and Z. morio-based diets showed dry matter
Potassium 750.6–773.0 970.0
ADC close to the reported values for fishmeal and soybean meal
Chloride 361.1–440.5 n.r.
for Nile tilapia (Fontes et al. 2019). At a 30% inclusion level, the
Iron 2.3–5.4 9.2
Zinc 2.5–8.2 8.3 Z. morio-based diet digestibility of dry matter, protein and lipid was
Copper 0.5–1.0 1.5 significantly lower than fishmeal digestibility for Nile tilapia juven-
Manganese 0.5–1.0 2.2 iles (Jabir et al. 2012a). When higher replacement levels or total fish-
Aluminum 4.6 n.r. meal replacement were evaluated in diets for Nile tilapia juveniles,
feed utilization, and body composition was not affected by up to
(n.r.) not reported. 25% replacement; however, higher replacement exerted an adverse
a
Values show the range of mean values from published sources (Finke 2002, effect on growth parameters, and this effect was attributed by the
2015; Araújo et al. 2019).
b
authors to the deficiency of these diets with reduced fishmeal levels
Source: Oonincx and Dierenfeld (2012).
to one or more essential amino acids present in fishmeal (Jabir et al.
2012b). To further improve the suitability of Z. morio meal diets,
their adulthood (Liu and Zhao 2019), and generally increasing pro-
Jabir et al. (2012c) supplemented a Nile tilapia diet in which 50% of
duction cost. Therefore, the potential of Z. morio adults as nutrient
fishmeal was replaced by Z. morio meal with various levels of mush-
source is limited in comparison to larvae. However, adults could be
room stalk meal (10, 15, and 20%) as a prebiotic and reported that
utilized for other applications, e.g., chitin extraction.
10% mushroom stalk meal inclusion positively affected growth per-
The variability observed among the results of the different studies
formance and particularly weight gain. Similar conclusions were also
regarding the body composition of Z. morio individuals may be due to
drawn for the suitability of hydrolyzed Z. morio meal for sea trout
the various diets used for its rearing (Payne et al. 2016, Oonincx and
(Salmo trutta m. trutta L.) fingerlings, as 10% hydrolyzed Z. morio
Finke 2020). Several studies with other insect species have shown that
meal inclusion ensured high survival rates and satisfactory growth
diet is a major determinant with regard to the insect body nutrient com-
performance and feed utilization parameters (Mikołajczak et al.
position (Oonincx and van der Poel 2010, Danieli et al. 2019). Although
2020). Recently, feeding trials with the gilthead sea bream (Sparus
data on the diet impact on Z. morio composition is limited, Latney et al.
aurata) have shown that Z. morio meal, even as full-fat or defatted,
(2017) showed variations in the calcium and phosphorus content, as
can be included in its diet at high inclusion levels replacing fishmeal
well as the metabolizable energy of Z. morio larvae, fed on four com-
protein up to 30% without any negative effects on fish growth per-
mercially available diets with different nutritive profiles, indicating the
formance and feed utilization (Asimaki et al. 2020, Karapanagiotidis
potential to manipulate their body composition by adjusting the feed
2020, personal communication).
based on the end-user requirements.

Poultry and Pigs

Besides aquafeeds, the inclusion of Z. morio meal or oil in poultry
Utilization as a Nutrient Source
diets has lately attracted considerable interest (Table 6). For in-
Fish stance, Benzertiha et al. (2020) studied the effect of the supple-
Although not listed in EU Regulation 2017/893 and therefore mentation of broiler chicken diets with small amounts (0.3%) of
not being officially authorized for inclusion in aquafeeds in EU, a Z. morio larvae full-fat meal, added ‘on top’ of a complete diet
number of studies have evaluated the effect of the partial replacement or calculated into diets, on the growth performance and selected
6 Journal of Insect Science, 2021, Vol. 21, No. 2

Table 5. Studies on the inclusion of Zophobas morio larvae meal (ZM) in fish diets

Animal species Life stage Duration % dietary inclusion Main outcome Reference

Oreochromis niloticus Fingerlings 56 d 30% Reduced digestibility of dry matter, Jabir et al. (2012a)
(Nile tilapia) protein and lipid of ZM-based
diets compared to fishmeal di-
gestibility
Oreochromis niloticus Fingerlings 56 d 7.5, 15, 22.5, and 30% Up to 25% of fishmeal can be Jabir et al. (2012b)
(Nile tilapia) (25, 50, 75, and 100% replaced by ZM without any
replacement of fishmeal) adverse effect on feed utilization
and body composition
Oreochromis niloticus Fingerlings 56 d 15% (50% fishmeal replace- Diet amendment with mushroom Jabir et al. (2012c)
(Nile tilapia) ment) + 10, 15 and 20% of stalk meal improved fish growth
mushroom stalk meal performance and survival

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Oreochromis niloticus Fingerlings 56 d 20% ZM showed dry matter ADC close Fontes et al. (2019)
(Nile tilapia) to the values reported for fish-
meal and soybean meal for Nile
tilapia
Oreochromis niloticus Fingerlings 84 d 15 and 30% (50 and 100% No negative effects on fish growth Alves et al. (2020)
(Nile tilapia) replacement of soybean performance. Lipid content
meal increase and protein content
decrease in fish fed the 30%
ZM-based diet
Salmo trutta m. trutta Fingerling 56 d 10% of hydrolyzed ZM (44% No adverse impacts on growth per- Mikołajczak et al.
(sea trout) fishmeal replacement) formance, feed utilization or gut (2020)
histomorphology
Sparus aurata (sea Fingerlings 100 d 5 and 10% (4.4 and 9.4% High survival rates. No adverse ef- Asimaki et al.
bream) fishmeal replacement) fect on feed intake, final weights, (2020)
specific growth rates and FCR

blood, and immune system traits of the birds. The authors reported Food
a positive effect on the body weight gain and feed intake, moreover, Additionally to the feed applications, the incorporation of Z. morio
there was a positive effect on the level of plasma immunoglobulins, larvae in food products has recently attracted scientific interest.
i.e., IgY and IgM. In a similar study, Benzertiha et al. (2019) evalu- Scholliers et al. (2019) explored the formulation of batter containing
ated the effect of Z. morio full-fat meal added in small amounts larvae from three insect species, i.e., T. molitor, A. diaperinus and
(0.2 and 0.3%) to a complete diet on the coefficients of apparent Z. morio, and concluded that based on the quality characteristics of
ileal digestibility, pancreatic enzyme activity, short-chain fatty acid the tested insect-based products Z. morio larvae show more potential
concentrations, bacterial enzymes, and microbiota community in for food applications. Similarly, Scholliers et al. (2020a, b) studied
the cecal digesta of broiler chickens and they did not report any the properties of hybrid meat products containing Z. morio larvae
negative effects on the nutrient ileal digestibility coefficients or to provide valuable insight into the composition and processing of
the activity of pancreatic enzymes. In the same study, dietary in- insect:meat applications and paving the way for the inclusion of
clusion of Z. morio full-fat meal was capable of improving the Z. morio larvae in insect-based food products.
health status of the birds by reducing pathogenic bacterial concen-
trations, such as those of the Bacteroides–Prevotella cluster and
Clostridium perfringens. In addition, this small amount of sup- Other Applications
plementation stimulated the gastrointestinal tract microbiota to Apart from an alternative nutrient source, Z. morio has been re-
produce enzymes, especially glycolytic enzymes. Similarly, the add- cently shown to be capable of eating, biodegrading and mineralizing
ition of small amount of Z. morio meal (0.2 and 0.3%) in broiler various types of plastics, as polystyrene or polyethylene (Miao and
diets has a prebiotic effect, as it increases the relative abundance Zhang 2010, Choi et al. 2020, Kim et al. 2020a, Li et al. 2020, Peng
of probiotic and commensal bacteria such as Actinobacteria in et al. 2020, Xu et al. 2020, Yang et al. 2020). For instance, Yang et al.
the cecal microbiome that act protectively against infections with (2020) demonstrated that Z. morio larvae could exclusively be fed
pathogenic bacteria (Józefiak et al. 2020). When soybean oil, the on styrofoam at a four-fold higher rate than the other plastic eating
most commonly used energy source ingredient in poultry diets, was tenebrionid T. molitor, and could ingest long-chain plastic molecules
totally replaced by oil obtained using super-critical CO2 extrac- and depolymerize them into low molecular-weight degraded com-
tion from Z. morio larvae, no adverse impact on the growth per- pounds. Furthermore, it is suggested that the larval gut microbiota
formance of broiler chicken and nutrient digestibility was noted contributes to plastic degradation, as the plastic-degrading cap-
(Kierończyk et al. 2018). ability of the larvae was inhibited when gut microbiota was sup-
Regarding pigs, only one study has evaluated to date the effect pressed by antibiotic treatment (Peng et al. 2020, Yang et al. 2020).
of Z. morio-based diets on these livestock animals. Briefly, Liu et al. In an effort to screen the plastic-degrading microbes of the larval gut
(2020) studied the effect of the supplementation of weanling piglet microbiota, several bacterial strains (e.g., Pseudomonas) have been
diets with 5% Z. morio powder, and reported improved amino acid isolated and is believed that are associated with the plastic-degrading
transportation in the intestine of pigs fed on the Z. morio containing ability of Z. morio larvae (Kim et al. 2020a, Li et al. 2020, Xu et al.
diets compared with the control corn–soybean basal diet. 2020). These new findings are of high importance for plastic waste
Journal of Insect Science, 2021, Vol. 21, No. 2 7

Table 6. Studies on the inclusion of Zophobas morio larvae meal (ZM) in poultry diets

Animal species Life stage Duration % Dietary inclusion Main outcome Reference

Broiler chicken 1-d old 28 d 5% replacement of soybean oil by Similar or better growth performance Kierończyk et al.
(Ross 308) ZM oil results compared to the soybean diet (2018 )
Broiler chicken 1-d old 35 d 0.2 and 0.3% amendment with ZM Body weight gain and feed intake Benzertiha et al.
(Ross 308) meal increase in dietary groups supple- (2019)
mented with ZM
Broiler chicken 1-d old 35 d 0.2 and 0.3% amendment with ZM Improved growth performance and Benzertiha et al.
(Ross 308) meal changes in selected immune system (2020)
traits
Broiler chicken 1-d old 35 d 0.2 and 0.3% amendment with ZM Commensal and probiotic microbiome Józefiak et al.
(Ross 308) meal composition modulated in the (2020)
cecum. Increase of the relative abun-

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dance of positive bacteria
Broiler chicken 1-d old 7d 0.4% of a fermented with Increase of average daily gain and Islam and Yang
(Ross 308) Lactobacillus plantarum and Immunoglobulin G and A levels, re- (2017)
Saccharomyces cerevisiae mixture duction of FCR, mortality and cecal
of 30% ZM larvae, 35% DDGSa, E. coli and Salmonella spp. contents
and 35% defatted rice bran

a
Distiller’s dried grains with solubles.

management and could offer a reliable solution to the problem of Yang (2016) proposed the use of probiotics from Z. morio larvae
plastic accumulation, which represents a global issue of major envir- as alternatives to antibiotics in broiler chicken. However, further re-
onmental importance. search is warranted to illuminate and unfold this potential. The pre-
The spectrum of Z. morio applications is continuously growing. biotic effect of other Z. morio-derived substances which are known
Recently, Du et al. (2020) showed that Z. morio hemolymph can to have antimicrobial activity, e.g., chitin, could be on the focus of
effectively protect bovine mammary epithelial cells against bacterial future research toward this direction.
infections and proposed Z. morio hemolymph as an efficient, alter- Safety issues should also been addressed with regard to the use
native therapeutic candidate for bovine mastitis, the most preva- and exploitation of Z. morio, in order to ensure food and feed safety.
lent disease affecting the dairy industry worldwide. Additionally, Studies on the potential microbiological risks that have to be con-
this species is often used as a model organism. Due to the fact sidered should be prioritized. Grabowski and Klein (2016) evaluated
that it is easily reared and is rich in fat, Gołębiowski et al. (2020) the microbiological quality of Z. morio larvae processed with four
used Z. morio larvae to study the effect of the entomopathogenic different drying techniques in order to identify the methods that can
fungus Metarhizium flavoviride (Gams and Rozsypal) (Hypocreales: ensure food quality and safety. Similarly, an evaluation of the safety
Clavicipitaceae) on the fat body lipid composition of insects, and re- of freeze-dried skimmed powder of Z. morio larvae revealed no ad-
ported qualitative and quantitative changes in the profiles of lipids in verse effect in oral toxicity tests in rats at doses up to 5,000 mg/kg/d
larvae of Z. morio due to the fungal infection. Previously, this species (Kim et al. 2020b). Such safety data should be examined into more
was used to study lipid metabolism and the endocrinological system detail and be adequately provided, in order to illustrate potential
of insects (Gołębiowski et al. 2014), offering a valuable model or- risks that may endanger human and animal health. The same counts
ganism to study various aspects of insect physiology. for potential Z. morio-related allergic responses that could be gener-
ated through consumption or inhalation of airborne insect-derived
material (Freye et al. 1996). However, the safety concerns related to
Future Research and Challenges Z. morio applications are not expected to be higher than the ones
Based on the above, the utilization of Z. morio as an alternative nu- described for other insect species currently commercially exploited
trient and protein source holds promises for the future. However, an (Van der Fels-Klerx et al. 2018).
essential prerequisite for the successful exploitation of this species To conclude, the so far available data classify Z. morio as a
as food and feed is the adjustment of the legislative framework that promising insect-based nutrient provider with great potential and
regulates the use of insects in food and feed applications. Within EU, future perspectives. Its comparative evaluation together with other
a first step could be the inclusion of Z. morio in the list of insect insect species has shown that Z. morio can adequately offer an al-
species that are allowed by EU Regulation 2017/893 to be included ternative to the species commonly used for this purpose so far (Van
in aquafeeds, whereas the approval of the insect use in poultry and Broekhoven et al. 2015, Adámková et al. 2016, Araújo et al. 2019).
swine diets, including Z. morio in the permitted species, would fur- Apart from its utilization in food and feed, it seems that this species
ther boost its utilization. can also be an effective waste management agent. Further research is
The route to the better exploitation of Z. morio comprehend needed to fully unfold the potential applications of this species and
several challenges. Apart of constituting solely a protein and nu- optimize its farming systems at an industrial scale. Considering that
trient source, the challenge is to illustrate the functional properties its relative T. molitor is already included in the list of ‘EU-authorized’
of Z. morio-derived diets. Zielińska et al. (2017) suggested that insect species for use in aquafeeds, future research should also focus
together with other insect species, Z. morio larvae are a valuable, on potential risk assessment aspects that can be further utilized by
largely unexploited source of antimicrobial peptides with antiradical regulatory and legislative authorities, toward the practical exploit-
activity, therefore, their consumption could potentially have an ation of this species for the applications mentioned in this work.
immune-triggering and health promoting effect. Similarly, Islam and Zophobas morio has the full potential of playing a significant role
8 Journal of Insect Science, 2021, Vol. 21, No. 2

in the future of insects as food and feed and research on this spe- W. H. Hendriks. 2013. The future supply of animal-derived protein for
cies should emphasize on highlighting the advantages of its use and human consumption. Trends Food Sci. Technol. 29: 62–73.
shading light on unexplored aspects that need to be considered. Bosch, G., S. Zhang, D. G. Oonincx, and W. H. Hendriks. 2014. Protein
quality of insects as potential ingredients for dog and cat foods. J. Nutr.
Sci. 3: e29.
Author Contributions Botella-Martínez, C., R. Lucas-González, J. A. Pérez-Álvarez, J. Fernández-
López, and M. Viuda-Martos. 2020. Assessment of chemical compos-
Both authors contributed equally to the conceptualization and writing of this ition and antioxidant properties of defatted flours obtained from several
review paper. edible insects. Food Sci. Technol. Int. [Published online ahead of print].
doi:10.1177/1082013220958854.
Boulos, S., A. Tännler, and L. Nyström. 2020. Nitrogen-to-protein conversion
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