Biochemical Systematics and Ecology 95 (2021) 104241

Contents lists available at ScienceDirect

Biochemical Systematics and Ecology
journal homepage: www.elsevier.com/locate/biochemsyseco

Carotenoids of hemipteran insects, from the perspective of
chemo-systematic and chemical ecological studies☆
Takashi Maoka a, *, Naoki Kawase b, Mantaro Hironaka c, Ritsuo Nishida daResearch Institute for Production Development 15 Shimogamo-morimoto-cho, Sakyo-ku, Kyoto, 606-0805, Japan
Minakuchi Kodomonomori Nature Museum 10 Kita-naiki, Minakuchi-cho, Koka, 528-0051, Japanc
Ishikawa Prefecture University, Bioresources and Environmental Sciences 305, Suematsu, Nonoichi-1, 921-8836, Japand
Kyoto University Yoshida-Honmachi, Sakyo-ku, Kyoto, 606-8501, Japanb

A R T I C L E I N F O

A B S T R A C T

Keywords:
Carotenoid
Hemiptera
Food chain
Chemo-systematics
Chemical ecology

Carotenoids of 47 species of insects belonging to Hemiptera, including 16 species of Sternorrhyncha (aphids anda whitefly), 11 species of Auchenorrhyncha (planthoppers, leafhoppers, and cicadas), and 20 species of Heter­
optera (stink bugs, assassin bugs, water striders, water scorpions, water bugs, and backswimmers), were
investigated from the viewpoints of chemo-systematic and chemical ecology. In aphids, carotenoids belonging to
the torulene biosynthetic pathway such as β-zeacarotene, β,ψ-carotene, and torulene, and carotenoids with aγ-end group such as β,γ-carotene and γ,γ-carotene were identified. Carotenoids belonging the torulene biosyn­
thetic pathway and with a γ-end group were also present in water striders. On the other hand, β-carotene,
β-cryptoxanthin, and lutein, which originated from dietary plants, were present in both stink bugs and leaf­
hoppers. Assassin bugs also accumulated carotenoids from dietary insects. Trace amounts of carotenoids weredetected in cicadas. Carotenoids of insects belonging to Hemiptera well-reflect their ecological life histories.

1. Introduction
Carotenoids are tetraterpene pigments that are distributed inphotosynthetic bacteria, some species of archaea and fungi, algae,
plants, and animals. About 850 naturally occurring carotenoids had
been reported up until 2018 (Britton et al., 2004; Maoka, 2019).
Photosynthetic bacteria, some species of archaea and fungi, algae, andplants can synthesize carotenoids de novo. However, as animals gener­
ally do not have carotenoid synthetic genes, they cannot synthesize
carotenoids de novo. Thus, carotenoids found in animals are either
directly accumulated from food or partly modified through metabolic
reactions (Liaaen-Jensen, 1998; Maoka, 2011).
Insects are the most diverse group of animals and they containvarious carotenoids. Most insects accumulate carotenoids that haveoriginated from plants through the food chain (Liaaen-Jensen, 1998;
Maoka, 2011; Maoka et al., 2020).
Hemiptera is an order of insects including Sternorrhyncha (aphids

and whiteflies), Auchenorrhyncha (e.g., planthoppers, leafhoppers, andcicadas), and Heteroptera (e.g., stink bugs and water striders). Most
hemipteran insects feed on plant sap using their sucking and piercing
mouthparts, and some of them are serious agricultural pests. On theother hand, some kinds of hemipteran insects such as assassin bugs andwater striders are carnivorous and mostly prey on insects. Some of theinsects belonging to Hemiptera have red, yellow, green, and blue-green
body colors.
Carotenoids without a plant origin, β-zeacarotene, β,ψ-carotene(generally called γ-carotene), torulene, β,γ-carotene, and γ,γ-carotene,
were identified in some species of aphids (Andrews et al., 1971; Britton
et al., 1977a, 1977b). These carotenoids are known to be characteristic
carotenoids in fungi. Therefore, they are considered to have originatedfrom endosymbiotic microorganisms such as fungi (Liaaen-Jensen,
1998). Recent investigations revealed that aphids synthesize caroten­
oids themselves by carotenoid synthetic genes, which are horizontallytransferred from fungi to aphids. Namely, the aphid genome itself☆
The results of functional identification of carotenoid biosynthesis genes that exist in the genome of the pea aphids Acrythosiphon pisum, with recombinant
Escherichia coli cells, and a part of carotenoid composition in aphids have been submitted to BMC Zoology by Takemura, M., Maoka, T., Koyanagi, T., Kawase, N.,
Nishida, R., Tsuchida, T., Hironaka, M., Ueda, T., and Misawa, N., as the title of ‘Elucidation of the whole carotenoid biosynthetic pathway of aphids at the gene level
and arthropodal food chain involving aphids and the red dragonfly’ (submitted September 22, 2020; under review January 2021).
* Corresponding author.
E-mail address: maoka@mbox.kyoto-inet.or.jp (T. Maoka).

https://doi.org/10.1016/j.bse.2021.104241
Received 23 November 2020; Received in revised form 21 January 2021; Accepted 23 January 2021
Available online 5 February 2021
0305-1978/© 2021 Elsevier Ltd. All rights reserved.

T. Maoka et al.

Biochemical Systematics and Ecology 95 (2021) 104241

encodes multiple enzymes for carotenoid biosynthesis. Red aphids havecarotenoid desaturase genes and synthesize torulene from phytoene bythemselves (Moran and Jarvik, 2010; Nováková and Moran, 2012;
Mandrioli et al., 2016; Ding B-Y et al., 2019). On the other hand,blue-green aphids synthesize polycyclic quinones using genes of theendosymbiotic bacterium Richettsiella (Tsuchida et al., 2010).
However, few reports have provided an overview of carotenoids inhemipteran insects (Andrews et al., 1971; Britton et al., 1977a, 1977b).
Especially, there are no reports on the carotenoids of Auchenorrhyncha
and Heteroptera. In the present paper, we describe the carotenoids in 47
species of insects belonging to Hemiptera, including 16 species of Ster­norrhyncha (aphids and whiteflies), 11 species of Auchenorrhyncha(planthoppers, cicadas, etc.), and 20 species of Heteroptera (stink bugs,etc.) from the viewpoints of comparative biochemistry and chemical
ecology.

from 200 to 600 nm using a photodiode-array detector (PDA). An Acq­uity 1.7 μm BEH UPLC C18 (2.1 id X 100 mm) column (Waters Corpo­
ration, Milford, CT, USA) was used as a stationary phase and MeCN:H2O(85:15) - MeCN:MeOH (65:35) (linear gradient 0–15 min) as a mobile
phase, at a flow rate of 0.4 mL/min for the HPLC system. Carotenoids
were identified by UV-VIS, MS, and MS/MS spectral data and retention
time in HPLC with comparison of authentic samples.
In the case of Acyrthosiphon pisum, carotenoids were isolated by silica
gel column chromatography followed by preparative HPLC and identi­
fied from UV-VIS, ESI TOF MS, 1H NMR, and circular dichroism (CD)
spectral data as described previous literature (Maoka et al., 2020). De­
tails of spectral data of γ,γ-carotene has not been reported (Britton et al.,2004). Therefore, spectral data of γ,γ-carotene was described here.
γ,γ-Carotene: ESI TOF MS (m/z) 536.4382 [M+] C40H56, Calcd for536.4404; UV-VIS (Et2O) 419, 439, 468 nm; 1H NMR δ (in CDCl3 at 500
MHz) 0.82 (6H, s, H-16, 16′ ), 0.90 (6H, s, H-17, 17′ ), 1.33 (4H, dd, J =14, 7 Hz, H-2, 2′ , 1.95 (6H, s, H-19, 19′ ), 1.97 (6H, s, H-20, 20′ ), 2.07
(4H, m, H-3, 3′ ), 2.29 (4H, m, H-4, 4′ ), 2.51 (2H, d, J = 9.5 Hz, H-6, 6′ ),4.57 (2H, br. s, H-18, 18′ ), 4.73 (2H, br. s, H-18, 18′ ), 5.84 (2H, dd, J =15.5, 9.5 Hz, H-7, 7′ ), 6.12 (2H, d, J = 11.5 Hz, H-10, 10′ ), 6.13 (2H, d, J
= 15.5 Hz, H-8, 8′ ), 6.24 (2H, m, H-14, 14′ ), 6.33 (2H, d, J = 15.5 Hz, H12, 12′ ), 6.61 (2H, dd, J = 15.5, 11.5 Hz, H-11, 11′ ), 6.63 (2H, m, H-15,15’). These spectral data were in agreement with published data (Arpin
et al., 1971; Britton et al., 2004).

2. Materials and methods
2.1. Insects
The following 47 species of insects belonging to Hemiptera werecollected in Koka City, Shiga Prefecture, Kyoto City, Kyoto Prefecture,
and Kanazawa City, Ishikawa Prefecture in Japan during April to
October. Sternorrhyncha (aphids and a whitefly, 16 species): Shivaphis
celti, Aphis gossypii, A. nerii, A. spiraecola, Semiaphis heraclei, Toxoptera
citricida, Acyrthosiphon pisum, Brevicoryne brassicae, Uroleucon for­mosanum, Uroleucon kikioensis, Macrosiphum euphorbiae, Megoura cras­sicauda, Lachnus tropicalis, Ceratovacuna nekoashi, Schlechtendaliachinensis, and Dialeurodes citri; Auchenorrhyncha (planthoppers, leaf­
hoppers, and cicadas, 11 species): Nilaparvata lugens, Hecalus prasinus,
Nephotettix cincticeps, Bothrogonia ferruginea, Platypleura kaempferi,
Cryptotympana atrata, C. facialis, Graptopsaltria nigrofuscata, Tannajaponensis japonensis, Hyalessa maculaticollis, and Meimuna opalifera;
Heteroptera (stink bugs, assassin bugs, water striders water scorpions,water bugs, and backswimmers, 20 species): Parastrachia japonensis,
Poecilocoris lewisi, Halyomorpha halys, Alcimocoris japonensis, Plautia stali,
Nezara antennata, Sastragala esakii, Acanthocoris sordidus, Haematoloecha
nigrorufa, Isyndus obscurus, Sirthenea flavipes, Corythucha marmorata,
Orius sauteri, Aquarius elongatus, A. paludum, Gerris latiabdominis, Met­
rocoris histrio, Ranatra chinensis, Appasus major, and Notonecta triguttata.
We identified each hemipteran specimen referencing from following
bibliographies: Enjyu (2013), Matsumoto (2008), Miyatake et al.
(1992), Saigusa et al. (2013) and Yasunaga et al. (1993).

3. Results and discussion
Fig. 1 shows structures of carotenoids found in hemipteran insects inthis study. Carotenoids in 47 species of insects belonging to Hemiptera,
including 16 species of Sternorrhyncha, 11 species of Auchenorrhyncha,
and 20 species of Heteroptera are shown in Table 1. Aphids contained
relatively higher levels of carotenoids among hemipteran insects.
Among them, Aphis nerii (242.1 μg/g), A. gossypii (192.7 μg/g), Semiaphis
heraclei (170.0 μg/g), and Megoura crassicauda (133.6 μg/g) contained
high levels of carotenoids. On the other hand, Uroleucon kikioensis,
Macrosiphum euphorbiae, and Ceratovacuna nekoashi contained low levels(less than 10 μg/g) of total carotenoids. Carotenoids were not detectedin Lachnus tropicalis. β-Carotene was found to be a major carotenoid(5.8–70.2% of total carotenoids) in many aphids. Carotenoids generated
by the torulene biosynthetic pathway such as β-zeacarotene,β,ψ-carotene, and torulene (Goodwin, 1980), were also present as major
carotenoids in many species of aphids. Torulene was also found in two
species of aphids: Brevicoryne brassicae (12.8%) and Aphis spiraecola(5.2%). Furthermore, carotenoids with a γ-end group (terminal methy­lene group in the C-5 end group, Arpin et al., 1971) such as β,γ-carotene,
γ,γ-carotene, and γ,ψ-carotene, were detected in all species of aphids as
major carotenoids (19.6–67.6%). Among them, β,γ-carotene was foundto be a major carotenoid (14.8–54.5%) in several species of aphids.
Whiteflies (Aleyrodidae) also belong to Stemorrhyncha. The citrus
whitefly, Dialeurodes citri, contained a very low level of carotenoids (0.5μg/g). β,ψ-Carotene was found to be a major carotenoid (more than 95%
of total carotenoids) in the citrus whitefly. Carotenoid compositions inaphids were markedly different from those in Auchenorrhncha andHeteroptera, as described later. It was reported that aphids synthesizedcarotenoid themselves by carotenoid synthetic genes, which were hor­izontally transferred from fungi to aphids. Namely, aphids synthesize
torulene from phytoene by carotenoid desaturase genes (Moran andJarvik, 2010; Nováková and Moran, 2012; Mandrioli et al., 2016; Ding
B-Y et al., 2019). As described above, β,ψ-carotene was the main
carotenoid in citrus whitefly, Dialeurodes citri. β,ψ-Carotene was notpresent in its host plant (Citrus unshiu). Sloan and Moran (2012) reported
that the tobacco whitefly B. tabaci synthesized carotenoid by employing
the genome of the obligate bacterial endosymbiont Portiera. Therefore,β,ψ-carotene in the citrus whitefly was also considered to be synthesized
by endosymbiotic bacteria.
Recently, our research group conduced a functional analysis of

2.2. Carotenoid extraction, analysis, isolation, and identification
The carotenoids were extracted from insects with acetone at room
temperature. After filtration, the acetone extract was partitioned withhexane:Et2O (1:1, v/v) and water. Then carotenoids were transferred tohexane:Et2O phase. The hexane:Et2O phase was washed with water anddehydrated on anhydrous sodium sulphate. The total carotenoid amount
were calculated using coefficient of E 1%cm = 2400 at λ max (Britton,
1995; Schiedt and Liaaen-Jensen, 1995).
Quantitative and qualitative carotenoid analyses were carried out
using our routine method using a high performance liquid
chromatography/photodiode-array detector/mass (LC/PDA/MS) sys­tem (Maoka, 2016; Maoka et al., 2020).
The LC/MS analysis of carotenoids was carried out using a Waters
Xevo G2S Q TOF mass spectrometer (Waters Corporation, Milford, CT,
USA) equipped with an Acquity UPLC system. The electro-spray ioni­
zation (ESI) time-of-flight (TOF) MS spectra were acquired by scanningfrom m/z 100 to 1,500 with a capillary voltage of 3.2 kV, cone voltage of
20 eV, and source temperature of 120 ◦ C. Nitrogen was used as anebulizing gas at a flow rate of 30 L/h. MS/MS spectra were measured
with a quadrupole-TOF MS/MS instrument with argon as a collision gas
at a collision energy of 20 V. UV-VIS absorption spectra were recorded
2

T. Maoka et al.

Biochemical Systematics and Ecology 95 (2021) 104241

Fig. 1. Characteristic carotenoids in Hemiptera. Photos: upper, Megoura crassicauda (Aphididae: Sternorrhyncha): lower. Poecilocoris lewisi (Scuttelleridae:
Hetrroptera).

carotenoid biosynthesis genes that existed in the genome of the pea
aphid Acrythosiphon pisum using recombinant Escherichia coli cells. As
the results, we found that a series of carotenoids with the torulene
biosynthetic pathway and β,γ-carotene were synthesized in E. coli
encoded by the carotenoid synthase/carotenoid cyclase gene sequencesfrom the aphid (Takemura et al., 2021; see footnote).
It is well-known that aphids feed on sap of phloem vessels in hostplants. However, characteristic carotenoids in plants such as lutein andzeaxanthin were not detected in aphids. These results indicate thataphids do not intake carotenoids from host plants but synthesize themthemselves by the carotenoid synthase/carotenoid cyclase gene hori­zontally transferred from fungi. Aphids are an important food ofcarnivorous insects and spiders and are called aeroplankton (Speight
et al., 2008). Thus, carotenoids characteristic to aphids have been foundin predatory dragonflies, beetles, and spiders, which potentially prey on
aphids through the food chain (Maoka et al., 2020).
On the other hand, carotenoids were not found in the aphid Lachnus
tropicalis, belonging to Lachninae. Quinons are present as the main
pigments in L. tropicalis. In Ceratovacuna nekoashi, belonging to Hor­maphidinae, quinines are present as the major pigments, whereas ca­
rotenoids are also present but only as minor pigments.
Contrary to aphids, carotenoid levels in Auchenorrhyncha (plan­
thoppers, leafhoppers, and cicadas) were very low, and carotenoids
produced by the torulene synthetic pathway and with a γ-end groupwere not present in these insects, as shown in Table 1. Planthoppers andleafhoppers are plant feeders that suck plant sap from grasses. β-Caro­tene, β-cryptoxanthin, and lutein, ingested from plants, were found to be
major carotenoids in planthoppers and leafhoppers: Nilaparvata lugens,
Bothrogonia ferruginea, Hecalus prasinus, and Nephotettix cincticeps. Greenand yellow body colors of planthoppers and leafhoppers were notextractable with organic solvents such as acetone and ethanol. There­
fore, these body colors were considered to be due to structural
coloration.
A low level of carotenoids (0.1–0.02 μg/g) was detected in cicadas,
Graptopsaltria nigrofuscata, Hyalessa maculaticollis, and Tanna japonensis
japonensis, whereas trace amounts of carotenoids were detected in otherspecies of cicadas (Table 1). β-Carotene and echinenone were found to
be major carotenoids. Cicadas ingest only xylem sap, which is essentially
free from carotenoids, throughout their life cycle. Therefore, caroten­
oids in cicadas might have originated from a symbiont, as in aphids.
β-Carotene, β-cryptoxanthin, lutein, and zeaxanthin were found to be

major carotenoids in both stink bugs and leafhoppers belonging toHeteroptera (Table 1). Among them, β-carotene was found to be a major
carotenoid (94.5–80.7%) in Sirthenea flavipes, Corythucha marmorata,
Haematoloecha nigrorufa, and Orius sauteri. Lutein was present as a major
carotenoid (74.0–40.0%) in Nezara antennata, Plautia stali, Halyomorphahalys, Alcimocoris japonensis, and Isyndus obsurus. Zeaxanthin (40.6%)
and its epoxide, antheraxanthin (34.6%), were present as major carot­
enoids in Parastrachia japonensis. They are characteristic carotenoids inplants. Stink bugs and leafhoppers also feed on sap of phloem vessels inplants. Stink bugs and leafhoppers might intake carotenoids from hostplants. P. japonensis displays a bright red body color. This red color could
not be extracted with organic solvent such as acetone and ethanol.
Therefore, it is considered to be due to structural coloration.(Britton
et al., 2008) (Manuta, 1948) (Seki et al., 1987).
Assassin bugs are carnivorous and prey on insects. β-Carotene,
β-cryptoxanthin, echinenone, and lutein, which were found in several
insects, were present in Isyndus obscurus. Therefore, these carotenoids
are considered to be of dietary origin.
Carotenoids in water striders (Gerridiae) belonging to Heteroptera
are shown in Table 1. Water striders contain relatively high levels ofcarotenoids (35.2–23.3 μg/g) among hemipteran insects. β,γ-Carotene,
γ,γ-carotene, β-zeacarotene, β,ψ-carotene, β-cryptoxanthin, and echine­none were found in water striders, Gerris latiabdominis, Aquarius elon­
gatus, A. paludum, and Metrocoris histrio, along with β-carotene as amajor carotenoid (about 60%). Water striders are carnivorous and often
feed on insects that fall onto the water surface. β-Carotene, β-cryptox­
anthin, and echinenone, are present in several insects (Maoka et al.,2020). Therefore, β-cryptoxanthin, echinenone, and a part of β-carotene
might be accumulated from prey insects that water striders have fed on.
On the other hand, β,γ-carotene, γ,γ-carotene, β-zeacarotene,β,ψ-carotene, and a part of β-carotene might be synthesized in water
striders themselves by carotenoid synthetic genes, which were hori­zontally transferred from fungi just as in aphids.
Notonecta triguttata (backswimmer), belonging to Notonectidae, isalso carnivorous and feeds on small fish, tadpoles, and several insects
that fall onto the water surface. β-Carotene was present as a major
carotenoid (72.2%) along with echinenone (4.5%) and β-cryptoxanthin(15.2%). Carotenoids with the γ-end group and belonging to the tor­ulene biosynthetic pathway were not present in this predatory species(Table 1).
Structures of carotenoids present in Hemiptera are shown in Fig. 1.
3

Auchenorrhyncha

4
Cicadidae

Heteroptera

CydnidaeScutelleridae
Pentatomidae

Acanthosomatidae
CoreidaeReduviidae
Tingidae
Anthocoridae
Gerridae

Nepidae
Belostomatidae
Notonectidae

sirex parasite
citrus white fly
brown rice planthopper
black-tipped leafhopper
spoon-headed leafhopper
green rice leafhopper
large brown cicada
robust cicada
evening cicada
elongate cicada
Kaempfer cicada
ground bug
red-striped golden stink bug
brown marmorated stink bug
Oriental stink bug
green stink bug
shieldbug
winter cherry bug
assasin bug
chrysanthemum lace bug
mulberry flower bug
water strider

Chinese water scorpion
giant water bug
three-spotted backswimmer

24.2
20.3

0.1
0.056
0.11
0.094
0.03

1.1
0.5
0.2
1.3

3.4
1.3
0.7
2.6
1.3
0.5
4.0
1.5
2.1

±
＋
31.2
50.2
74.2
~100
80.5
~100
±
±
±
2.5
25.5
14.8
10.0
13.2
42.2
65.8
＋
83.1
33.5
94.5
82.1
80.7
65.5
58.9
60.5
60.1
95.0
50.1
72.2

14.2

30.4

33.5
17.6
7.3
55.2
28.3
>95

5.2

12.8

14.8
23.6
54.5
25.1
33.7
22.4
15.9
33.8
38.8
42.2
4.9
48.8
18.1
1.2

6.4
11.0
3.2
13.1

2.1
2.2
7.5

3.7
10.0

1.2
12.0

11.6

2.3

4.3

13.7

7.9
12.6
1.1
5.1
10.6
0.3
6.8
11.4
8.3
0.5
2.5
13.7

1.5
3.7

3.3

15.7

＋
22.1
35.5

＋
43.8
13.5

2.9
0.8
10.1

5.5

14.0

2.0

5.6
2.5
1.2

4.3
2.3
2.3
1.5

8.1
2.8
6.6
5.2

*1:Drepanosiphinae, *2-1: Aphidinae (Aphidini), *2-2: Aphidinae (Macrosiphini), *3: Lachninae, *4: Hormaphidinae, *5: Eriosomatinae.
The list of hemipteran insects in Table 1 were referenced from Hayashi et al. (2016) and Yano (2018).

3.2
11.5
7.3
11.8

2.6
5.4
3.3
1.2

Unidentified

Lutein epoxide

LuteinAntheraxanthin

Zeaxanthinβ-Cryptoxanthin

Echinenone

γ,ψ-Carotene

13.5
44.6
11.0
14.2
11.2
32.5
2.2

γ,γ-Carotene

51.6
0.5
2.1
32.9
1.8
20.5

β,γ-Carotene

β,ψ-Carotene

5.8
18.7
18.2
12.1
22.1
24.3
70.2
20.0
19.4
25.8
71.1
19.5

Torulene

β-Zeacarotene

large chestnut aphid

β,β-Carotene

*3
*4
*5
Aleyrodidae
Delphacidae
Cicadellidae

potato aphid

26.5
192.7
242.1
90.2
170.0
14.4
39.7
52.0
72.7
2.8
5.3
133.6
N.D.
2.2
12.8
0.5
±
＋
2.4
0.1
0.022
0.15
0.11
0.009
±
±
±
6.0
1.3
1.2
19.2
27.0
6.3
19.2
＋
3.4
5.7
4.6
34.2
2.1
23.3
26.7
35.2
23.3
9.5
3.0
20.9

(µg/Specimen)

Species*2-2

cotton aphid
oleander aphid
Spiraea aphid
celery aphid
citrus brown aphid
pea aphidcabbage aphid
Formosan hairy aphid

Total Carotenoid (µg/g)

FamilyShivaphis celti
Aphis gossypii
A. nerii
A. spiraecola
Semiaphis heraclei
Toxoptera citricida
Acyrthosiphon pisum
Brevicoryne brassicae
Uroleucon formosanum
U. kikioensis
Macrosiphum euphorbiae
Megoura crassicauda
Lachnus tropicalis
Ceratovacuna nekoashi
Schlechtendalia chinensis
Dialeurodes citri
Nilaparvata lugens
Bothrogonia ferruginea
Hecalus prasinus
Nephotettix cincticeps
Graptopsaltria nigrofuscata
Hyalessa maculaticollis
Tanna japonensis
Cryptotympana facialis
C. atrata
Meimuna opalifera
Platypleura kaempferi
Parastrachia japonensis
Poecilocoris lewisi
Halyomorpha halys
Alcimocoris japonensis
Plautia stali
Nezara antennata
Sastragala esakii
Acanthocoris sordidus
Haematoloecha nigrorufa
Isyndus obscurus
Sirthenea flavipes
Corythucha marmorata
Orius sauteri
Aquarius elongatus
A. paludum
Gerris latiabdominis
Metrocoris histrio
Ranatra chinensis
Appasus major
Notonecta triguttata

Common nameSuborderAphididae *1
*2-1

3.1
4.4
4.2
2.3
4.5

15.2
4.5
15.4
10.1
12.5
12.4
10.5
4.5
25.2
15.2

40.6
24.5
2.0
45.0
20.2
5.6
14.2

34.6
35.5

5.4

74.0
45.0
50.5
40.6
15.3

7.5
9.2

8.5
40.5

3.5

13.7

6.1

11.1

20.3
14.5
9.2
1.8

10.5
4.4
2.2
0.9
0.4
1.0
0.7
3.9
3.1
2.2
3.4
7.4
0.5
7.5
8.1

Biochemical Systematics and Ecology 95 (2021) 104241

Sternorrhyncha

T. Maoka et al.

Table 1
Carotenoids in 47 species of insects belonging to Hemiptera.

T. Maoka et al.

Biochemical Systematics and Ecology 95 (2021) 104241

As described above, aphids contained characteristic carotenoids, whichwere synthesized by carotenoid synthase/carotenoid cyclase genes
horizontally transferred from fungi, whereas carotenoids from hostplants were not detected. On the other hand, stink bugs and leafhoppers
possess carotenoids, likely from host plants. Furthermore, both types ofcarotenoids were present in water striders. β-Carotene was scarcely
detected in cicadas.
Carotenoids are widely distributed in insects and play importantfunctional roles such as a photo-protector, an antioxidant, and for pro­tective coloration (Shamim et al., 2014). Most insects acquire caroten­
oids from foods and accumulated them in their body (Maoka et al.,2020). Aphids are sap-feeding insects that cannot intake carotenoids
from their host plants but acquire the ability to synthesize them bycarotenoid synthetic genes from symbiotic fungi, as described above. On
the other hand, some aphids biosynthesize quinine pigments, which playa role as a photo-protector as carotenoids (Shamim et al., 2014).
Therefore, Lachnus tropicalis and Ceratovacuna nekoashi, which lack ca­
rotenoids, might not need carotenoids for such a purpose.
Carotenoid contents in planthoppers, leafhoppers, stink bugs, andassassin bugs are very low, as shown in Table 1, since the body color ofthese insects is due to structural coloration. Therefore, they may notneed to accumulate large amounts of carotenoids.
Cicadas spend a large part of their life histories in their nymphal
stage underground. Therefore, photoprotectors, such as carotenoids andquinines may not be needed in their larval stage. During adult molting,they rapidly synthesize melanins (Asano, 2013), which may play a role
as a protector against sunlight instead of carotenoids or quinines.
In conclusion, carotenoids of Hemiptera well-reflect their ecologicallife histories.

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Author statement
TM conceived this research and carried out carotenoid analysis. N.K.,
M.H, and R.N. collected insects samples and discussed the systematics
and ecological history of insects.
Declaration of competing 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.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.bse.2021.104241.
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