life
Review
Pygidial Glands in Carabidae, an Overview of Morphology and
Chemical Secretion
Anita Giglio 1, * , Maria Luigia Vommaro 1 , Pietro Brandmayr 1
1
2
*
and Federica Talarico 2
Department of Biology, Ecology and Earth Science, University of Calabria, 87036 Rende, Italy;
marialuigia.vommaro@unical.it (M.L.V.); pietro.brandmayr@unical.it (P.B.)
Natural History Museum and Botanical Garden, University of Calabria, 87036 Rende, Italy;
federica.talarico@unical.it
Correspondence: anita.giglio@unical.it; Tel.: +39-0984492982; Fax: +39-0984492986
Abstract: Predator community structure is an important selective element shaping the evolution of
prey defence traits and strategies. Carabid beetles are one of the most diverse families of Coleoptera,
and their success in terrestrial ecosystems is related to considerable morphological, physiological, and
behavioural adaptations that provide protection against predators. Their most common form of defence is the chemical secretion from paired abdominal pygidial glands that produce a heterogeneous
set of carboxylic acids, quinones, hydrocarbons, phenols, aldehydes, and esters. This review attempts
to update and summarise what is known about the pygidial glands, with particular reference to the
morphology of the glands and the biological function of the secretions.
Keywords: allomone; chemical ecology; defensive secretion; gas chromatography; ground beetles;
microscopy; morphology
Citation: Giglio, A.; Vommaro, M.L.;
Brandmayr, P.; Talarico, F. Pygidial
Glands in Carabidae, an Overview of
Morphology and Chemical Secretion.
Life 2021, 11, 562. https://doi.org/
10.3390/life11060562
Academic Editor: Dmitry L. Musolin
Received: 18 May 2021
Accepted: 12 June 2021
Published: 15 June 2021
Publisher’s Note: MDPI stays neutral
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Copyright: © 2021 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
1. Introduction
The carabid beetles (Coleoptera, Carabidae) include approximately 40,000 described
species that are ecologically important as predators in many ecosystems and range in
feeding habits from generalist to specialists [1,2]. Carabids are often used as indicators
because they are extremely sensitive to environmental changes [3–5]. Their ecological role
in the trophic web of agroecosystems [6], makes them particularly suitable for monitoring
the impact of agrochemicals [5,7,8] and heavy metals [9–13]. Furthermore, as generalist
predators, ground beetles provide important ecosystem services by lowering populations
of invertebrate pests and weed seeds [14,15]. However, carabids are consumed by a number
of different species, including invertebrates and insectivorous vertebrates such as birds,
mammals, amphibians, and reptiles [1]. Predator–prey interactions are likely the major
driving force for the evolution of defences against predators in carabid beetles. Strategies
to escape predatory attacks primarily include morphological adaptations, such as cryptic
or warning coloration [16–19] and dorso-ventral flattening, large eyes, and long legs to
escape [20], as well as secretion of chemical repellents [21–23]. Ground beetles possess a
pair of abdominal glands called pygidial glands that produce defensive secretions. The
main function of the pygidial glands is to defend against predators, but they also engage in
biological activities such as facilitating the penetration of the defensive substances into the
integument of the predator and inhibiting the growth of fungi and pathogens [24,25]. A few
studies to date have examined the chemical compounds of pygidial gland secretions [26–30]
and comparatively investigated their taxonomic significance [22,31–34]. We attempt to
review the current state of knowledge on the pygidial glands of carabid beetles by providing
an overview of their structure and the chemical compounds of the secretion.
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
Life 2021, 11, 562. https://doi.org/10.3390/life11060562
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Life 2021, 11, 562
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2. General Morphology
Forsyth [35] first proposed a comparative description of pygidial glands in 71 species
from 34 tribes to define phylogenetic relationships within Carabidae. Currently, approximately 150 species from 43 tribes have been described (Table 1). The most commonly used
examining technique to study pygidial gland morphology is light microscopy (LM). In addition, other techniques such as fluorescence (FM) microscopy, scanning electron microscopy
(SEM) and focused ion beam/scanning (FIB/SEM) electron microscopy, (TEM) transition electron microscopy, synchrotron radiation X-ray phase-contrast micro-tomography
(SR-PhC micro-CT) are also applied.
Each pygidial gland consists of a variable number of secretory lobes (acini), collecting
duct, reservoir chamber, reaction chamber, and efferent duct (Figure 1). These glands (class
3 according to the classification of Noirot and Qhennedey [36,37]) are variable in structure
and have been described in several species [35,38]. The lobe or acinus, which is spherical or
elongated and enveloped in a thin basal lamina, is a cluster of secretory units, connected to
the collecting duct by a conducting duct that drains secretions outward. The secretory unit
consists of two parts, an elongated, cube-shaped secretory cell surrounding a receiving duct
and a duct cell surrounding the conducting duct [35,39–41]. The receiving duct is a porous
tube composed of one or more layers of epicuticle located in its extracellular space and
bounded by microvilli. The collecting duct has an epithelial wall of flattened cells, lined by
endocuticle, and a thin layer of epicuticle that is regularly folded into spiral ridges, annular
arrays, or pointed peg-like projections, that reduce the volume of the lumen to control the
free flow of secretion to the reservoir chamber [35,39,41]. The entrance of the collecting duct
to the reservoir chamber is of great variability. It is located at the anterior or middle position
in Scaritinae, Brachininae, and some Bembidiini, Pterostichini, Amarini, Carabini, Nebriini,
Metriini, and Paussini [33,35,39,40,42–44]. While it is located near the entrance of the
efferent duct in Harpalini, Agonini, Chlaeniini, Dryptini, Anthiini, Lebiini, Trachypachini,
Omophronini, Loxandrini, Catapieseini, Galeritini, and Zuphini [31,33,35,45]. The reservoir
chamber is a spherical, elongate, or bilobate compartment of variable size. Interwoven
muscle bundles cover the outer wall and are connected to tracheal branches. The basal
membrane supports flattened epithelial cells covered by a thin uniform layer of endo- and
epicuticle. The muscular contraction regulates secretion through a valve that separates
the reservoir from the reaction chamber. In Paussinae, Brachininae, and Carabinae, an
accessory gland is located below the valve [35]. Secretions from the reservoir chamber
are mixed with secretions from the accessory glands in the reaction chamber. The efferent
duct leads from the reservoir chamber to the external orifice. The close association of the
pygidial glands with the tracheal branches suggests a high aerobic metabolism.
The external orifice is located dorso-laterally in the posterior part of the abdomen,
near to the antero-lateral margin of the ninth tergite, and close to the tergo-sternal suture
in Carabinae, Scaritinae, Paussinae, Elaphrinae, Broscinae, and Brachinini, or at the posterolateral margin of the eighth tergite in derived lineages, e.g., Trechinae and Harpalinae,
and including Licinini, Chlaeniini, Panagaeini, Anthiini, Zabrini, Oodini, Pterostichini,
and Agonini [35,46]. Differences in pygidial gland morphology between sexes have been
reported in Cicindela campestris [47].
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Figure 1. Schematic drawing of a pygidial gland. cd: collecting duct; ed: efferent duct; r: reservoir
chamber; rc: reaction chamber; sl: secretory lobe; VIII: eighth tergite; IX: ninth tergite (for more
details of species listed in the text, see Forsyth (1972) [35]).
Table 1. Summary of carabid species in which the pygidial gland morphology has been investigated and the method used
for analyses. Abbreviations—CLSM: confocal laser scanning microscopy; FIB/SEM: focused ion beam/scanning electron
microscopy; FM: fluorescence microscopy; LM: light microscopy; NLM: non linear microscopy; SEM: scanning electron
microscopy; SR-PhC micro-CT: synchrotron radiation X-ray phase-contrast micro tomography.
§
Tribe
Genus
Species
Methodology
Refs
Metriini
Ozaeniini
Paussini
Metrius
Sinometrius
Mystropomus
Paussus
Cicindelinae
Cicindelini
Heteropaussus
Cicindela
Carabinae
Carabini
Calosoma
M. contractus
S.turnai
M. regularis
P. favieri
P. laevifrons
H. jeanneli
C. campestris
C. hibrida
C. oceanicum
C. schayeri
C. senegalense
C. sycophanta
C. (Tomocarabus) convexus
C. (Procustes) coriaceus
C. problematicus
LM; FIB/SEM
LM; FIB/SEM
LM
LM; FM; FIB/SEM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
[35,39]
[39]
[34]
[40]
[35]
[35]
[47]
[47]
[34]
[34]
[35]
[48]
[42]
[42,49]
[35]
Subfamily
Paussinae
Carabus
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Table 1. Cont.
§
Subfamily
Tribe
Genus
Cychrus
Pamborus
Elaphrus
Blethisa
Loricera
Omophron
Eurynebria
Leistus
Nebria
Elaphrinae
Cychrini
Pamborini
Elaphrini
Loricerinae
Omophroninae
Nebriinae
Loricerini
Omophronini
Nebriini
Scaritinae
Notiophilini
Clivinini
Notiophilus
Clivina
Dyschiriini
Pasimachini
Schizogenius
Dyschirius
Pasimachus
Carenini
Carenum
Broscinae
Broscini
Laccopterum
Philoscaphus
Eurylychnus
Trechinae
Trechini
Bembidiini
Promecoderus
Thalassotrechus
Trechus
Bembidion
Patrobinae
Patrobini
Amblytelus
Patrobus
Harpalinae
Morionini
Morion
Moriosomus
Diploharpus
Loxandrus
Perigonini
Loxandrini
Sphodrini
Pterostichini
Oxycrepis
Calathus
Pristonychus
Abacomorphus
Abaris
Blennidus
Castelnaudia
Cratoferonia
Cratogaster
Cyclotrachelus
Gasterllarius
Incastichus
Loxodactylus
Myas
Notonomus
Species
Methodology
Refs
C. ullrichii
C. (Megodontus) violaceus
C. caraboides rostratus
P. alternans
E. cupreus
B. multipunctata
L. pilicornis
O. dentatum
E. complanata
L. ferrugineus
N. brevicollis
N. psammodes
N. substriatus
C. basalis
C. collaris
C. fossor
S. lineolatus
D. globosus
P. elongatus
P. subsulcatus
C. bonelli
C. interruptum
C. tinctillatum
L. foveigerum
P. tuberculatus
E. blagravei
E. ollifi
P. sp.
T. barbarae
T. obtusus
B. lampros
B. rupestre
A. curtus
P. longicornis
P. septentrionis
M. simplex
M. seticollis
D. laevissimo
L. icarus
L. longiformis
L. velocipes
O. sp.
C. ambiguus
P. terricola
A. asperulus
A. anaea
B. liodes
C. superba
C. phylarchus
C. melas
C. sigillatus
G. honestus
I. aequidianus
L. carinulatus
M. coracinus
N. angusribasis
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
[49]
[43]
[35]
[34]
[35]
[35]
[35]
[35]
[35]
[35]
[35]
[50]
[35]
[34]
[35]
[35]
[31]
[35]
[35]
[51,52]
[34]
[34]
[34]
[34]
[34]
[34]
[34]
[34]
[35]
[35]
[28,35]
[35]
[34]
[31]
[35]
[31]
[31]
[31]
[31]
[34]
[31]
[31]
[35]
[35]
[34]
[31]
[31]
[34]
[34]
[34]
[31]
[31]
[31]
[34]
[31]
[34]
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Table 1. Cont.
§
Subfamily
Tribe
Genus
Prosopogmus
Pseudoceneus
Pterostichus
Species
Methodology
Refs
N. crenulatus
N. miles
N. muelleri
N. opulentus
N. rainbowi
N. scotti
N. triplogenioides
N. variicollis
P. harpaloides
P. iridescens
P. (Cophosus) cylindricus
P. (Monoferonia) diligendus
P. externepunctatus roccai
P. fortis
P. luctuosus
P. madidus
P. melanarius
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM; NLM
LM
LM
LM
LM
LM
LM
SR-PHC
MICRO-CT
LM; NLM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM; NLM
LM
LM
LM
CLSM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
[34]
[34]
[34]
[34]
[34]
[34]
[34]
[34]
[34]
[34]
[44]
[31]
[50]
[33]
[31]
[38]
[35]
P. melas
Platynini
Zabrini
Molopini
Harpalini
Licinini
Chlaeniini
Rhytisternus
Sarticus
Sphodrosomus
Trichosternus
Agonum
Amara
Curtonotus
Zabrus
Abax
Molops
Bradycellus
Diaphoromerus
Harpalus
Pseudophonus
Badister
Dicrochile
Licinus
Syagonix
Chlaenius
Oodes
Panagaenini
Masoreini
Odacanthini
Craspedophorus
Panagaeus
Psecadius
Tefflus
Masoreus
Colliuris
P. (Pseudomaseus) nigrita
R. laevilaterus
S. cyaneocinctus
S. saisseri
T. nudipes
A. dorsale
A. aenea
C. fulvus
Z. tenebriodes
A. parallelepipedus (sub:A. ater)
M. (Stenochoromus)montenegrinus
B. harpalinus
D. edwardsi
H. aeneus
H. pensylvanicus
P. rufipes (sub:pubescens)
B. bipustulatus
D. brevicollis
D. goryi
L. depressus
S. blackburni
C. australis
C. cumatilis
C. inops
C. pallipes
C. velutinus
C. vestitus
O. amaroides
O. hehpioides
C. sp.
P. crux-major
P. eustalactus
T. sp.
M. wetterhlii
C. melanura
C. pensylvanica
[53]
[44]
[34]
[34]
[34]
[34]
[35]
[35]
[35]
[35]
[35,49]
[44]
[35]
[34]
[35]
[54]
[35]
[35]
[34]
[34]
[35]
[34]
[34]
[35]
[33]
[33]
[50]
[35,50]
[31]
[35]
[34]
[35]
[35]
[35]
[35]
[35]
[31]
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Table 1. Cont.
§
Tribe
Genus
Species
Methodology
Refs
Lebiini
Galeritini
Anthiini
Helluonini
Dercylini
Catapieseini
Eudalia
Metabletus
Movmolyce
Galerita
Anthia
Helluo
Dercylus (s.s.)
Catapiesis
Dryptini
Drypta
E. macleayi
M. foveatus
M. phyllodes
G. lecontei
A. artemis
H. costatus
D. sp.
C. attenuata
C. sulcipennis
D. dentata
D. japonica
S. colymbeioides
A. bombarda
A. crepitus
A. displosor
B. crepitans
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM
LM; FM; FIB/SEM
LM; FM; FIB/SEM
LM
LM
LM; FM; FIB/SEM;
SEM
LM; FM; FIB/SEM
LM
LM
LM; FM; FIB/SEM
LM; FM; FIB/SEM
LM
LM; FM; FIB/SEM
LM
[34]
[35]
[35]
[45]
[35]
[34]
[31]
[31]
[31]
[35]
[33]
[34]
[41]
[41]
[35]
[35]
Subfamily
Brachininae
Pseudomorphini
Brachinini
Sphallomorpha
Aptinus
Brachinus
B. elongatus
Pheropsophus
§
B. sclopeta
B. stenoderus
P. verticalis
P. africanus
P. hispanus
P. lissoderus
P. occipitalis
P. verticalis
[41,55]
[41]
[33]
[34]
[41]
[41]
[35]
[41]
[34]
Classification of taxa has been arranged according to Bousquet [56] and Beutel and Ribera [57].
3. Excretory Mechanisms
Oozing, spraying, and crepitation are the main types of external excretory mechanisms
observed in carabid beetles in response to disturbance [58]. Oozing of secretion over the
cuticle of the hind segments occurs in species that have relatively weakly developed
muscles on the wall of the reservoir chamber, i.e., in the tribes Nebriini, Notiophilini,
Loricerini, Elaphrini, and the subfamilies Scaritinae, Cicindelinae, and Broscinae [32,35].
This is probably the plesiomorphic mode of discharge, whereas the secretion expelled
by strong muscle pressure on the reservoirs is an apomorphic adaptation. The discharge
of a directional secretion by turning the tip of the abdomen has been observed in many
taxa that exhibit a variable secretion discharge, such as Trechini, Bembidiini, Galeritini,
Carabini, Cychrini, Harpalini, Agonini, Anthiini, and Pterostichini (except the genus
Abax) [32,45,59]. Bombardier beetles discharge secretion by crepitation [60,61], with the
exception of Metrius contractus, which discharges its secretion using the oozing ancestral
discharge mechanism [39,62]. This discharge has evolved independently in Ozaenini
and Paussini on the one hand and in Brachinini on the other. In the tribe Brachinini, the
explosive defence is an active enzymatic exothermic reaction that produces benzoquinones,
free oxygen, water, and heat up to 100 ◦ C [55]. The process begins with muscle contraction
of the reservoir chamber, which allows stored hydroquinones and hydrogen peroxide,
to move through the one-way valve, enter the reaction chamber, and mix with catalases
and peroxidases produced by the accessory glands. In Paussinae, fluids are directed via
a cuticular fold (Coanda flange) located at the posterolateral angle of the elytra, which
serves as a launching guide for rapid anterior discharge [60,61,63]. The ability to direct the
sprayed secretion has also been observed in Calosoma prominens [64].
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4. Chemical Compounds of Secretion
To date, over 363 species from 45 tribes have been studied by gas chromatographymass spectrometry (GC-MS) (Table 2) in dichloromethane or hexane extracts. The semiochemicals, listed in Table 2, belong to one of the following classes: aliphatic and aromatic
carboxylic acids, phenols (m-cresol and xylenol), aldehydes, quinones, hydrocarbons, ketones, terpenes, and esters. The biosynthetic pathways of these compounds have been
extensively studied in arthropods [27,65]. However, studies addressing their biogenesis in
the pygidial gland of carabids are lacking. The enzymatic derivation of quinones is one
of the few metabolic pathways investigated. The bombardier beetle Brachinus elongatulus
has the ability to convert m-cresol to 2-methyl-1,4-hydroquinone, which is then oxidised to
2-methyl-1,4-benzoquinone (toluquinone), within 24 h in its defensive spray, when added
to food or injected into the haemocoel [66]. An origin from amino acids has been demonstrated for carboxylic acids. Valine is converted into methacrylic and isobutyric acids in
Carabus taedatus [67] and Scarites subterraneus [68]. Biosynthesis of both tiglic and ethacrylic
acid from isoleucine via 2-methylbutyric acid has been demonstrated in Pterostichus californicus [69]. Indeed, valine and isoleucine are essential amino acids, diet-dependent and
strictly regulated by the availability of resources [70].
4.1. Interspecific Adaptations
The chemical composition of pygidial gland secretions exhibits interspecific variability
within and among subfamilies (Table 2). This variability is the result of a trade-off between
the diversity of predators in different habitats and the fitness costs of resource allocation in
life traits such as behavioural defences against these enemies [2,71].
The chemicals found in secretions belong to two different functional categories, allomones and bacteriostats. Allomones are primarily involved in the secondary antipredator responses that carabids exhibit as prey to actively defend themselves against predators. Ground beetles emit volatile substances directed at specific groups of arthropods
or vertebrates that act as repellents on the chemoreception of predators or interfere with
physiological processes as irritants (emesis, vesication) [58]. Deterrent, toxic, and irritant
properties of pygidial gland secretions are known in bombardier beetles (Brachinini), which
release irritant quinones by a hot, pulsed spray mechanism [55,61,66] as an antipredator
defence [72,73]. Quinones are the main class of compounds also found in the secretions
of obligate or facultative myrmecophilous species belonging to Metrini, Ozaenini, and
Paussini [34,74]. In the defensive secretions of Clivinini [75] and Metrius contractus [62],
they are associated with complex mixtures of monoterpenes or hydrocarbons (Table 2).
Saturated and unsaturated aliphatic carboxylic acids and fatty acids are widely distributed
in the subfamilies Carabinae, Loricerinae, Nebrinae, Scaritinae, Scaritinae, and Harpalinae.
They are recorded as a separate compound class in some species that belong to the tribes
Pamborini, Elaphrini, Loricerini, Omophronini, Notiophilini, Broscini, Patrobini, Sphodrini,
Pterostichini, Platynini, Harpalini, Licinini, and Lebiini. In Cychrini, irritant carboxylic
acids (i.e., methacrylic acid) and fatty acids (i.e., tiglic acid) are released, associated with
a stridulatory elytra-abdominal mechanism acting as an acoustic warning signal against
predators [76,77]. Behavioural analyses showed that Pasimachus subsulcatus (Scaritinae)
secretes a mixture of methacrylic acid and fatty acids to protect itself from lizards [51,52].
Carboxylic acids are also found in variable associations with terpenes, quinones, and hydrocarbons in Trechinae, and Harpalinae (Table 2). The repellent effect of salicylaldehyde
in the secretion of Calosoma prominens has been tested against ants and vertebrates [64].
This chemical has also been detected in C. sycophanta, C. schayeri, C. oceanicum [34,48], C.
prominens [64], C. chinenses [33], Loxandrus longiformis [34], and Bembidion quadriguttatum, A.
flavipes [78] in a mixture with carboxylic acids. Benzaldehyde is the typical component of
secretion in Cicindelinae [79,80]. It is produced via a cyanogenetic pathway that is absent
in the other carabid subfamilies [81]. In tiger beetles, secretion of benzaldehyde may be associated with several antipredator characters, including aposematic camouflage, flight, and
gregarious behaviour to avoid predators such as robber flies, lizards, and birds [17,82,83].
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Synergism between polar volatile irritant compounds and lipophilic components of
secretion has been demonstrated. Nonpolar lipophilic components from Galerita lecontei
(long-chain hydrocarbons and esters) act as wetting and penetration enhancers and facilitate
the spread of volatile polar compounds such as formic and acetic acids in the cuticle of
predators [45]. In Helluomorphoides clairvillei, n-nonyl acetate facilitates the spread of
formic acid through the epidermis or cuticle of predators [84]. The same surfactant effect
has been attributed to hydrocarbons [85] for the uptake of repellent quinones in Metrius
contractus [62].
The mixture of substances in glandular secretions also has biological functions. In vitro
assays have shown that the pygidial gland secretion inhibits cell proliferation [86]. The mixture of aromatic (benzoic acid) and aliphatic carboxylic acids, esters, and terpenes have antimicrobial and fungicidal activity in Carabus ullrichii, C. coriaceus, Abax parallelepipedus [49],
caterpillar hunter Calosoma sycophanta [48], and troglophilic and guanophilic Laemostenus
(Pristonychus) punctatus [87]. Complex mixtures of monoterpenes are found in the defensive
secretions of a large number of the species reported here (Table 2). Terpenes are volatile
and are present in glandular secretions of many taxa, acting as chemical deterrents, trail
scents, mating attractants, or alarm pheromones [22]. In carabid beetles, they have also
been detected in the pupal stages of Carabus lefebvrei [88].
4.2. Intraspecific Adaptations
Little is known about intraspecific variation in secretion as a function of sex, age, and
resource availability. Nevertheless, data collected to date suggest that chemical secretion
plays a parsimonious role in both antipredation and mating behaviour. In Oodes americanus,
defensive secretion shows qualitative differences in males and females [89]. The sexual
dimorphism of carboxylic acids found in the defensive secretion of Chlaenius cordicollis
depends on the reproductive status and age of both sexes and provides a means of chemical
communication between the sexes [89,90]. Sex-specific variation likely protects mates
during copulation, and the flower number of compounds in female secretions saves females
the cost of synthesising them [90]. Although compounds that act as pheromones, such as
pentacosadiene, 7-hexyldocosane, 9-methyltetracosane, have been detected in Laemostenus
punctatus, Trachypachus gibbsi, and Helluomorphoides clairvillei, studies on their role in alarm
or sex-aggregation reproductive behaviour are limited [27].
Intra- and inter-population variation in defensive secretion has also been documented
to reflect genetic variability at the population level in responses to selective habitat pressure,
as observed in Chaenius cordicollis [91], Pasimachus subsulcatus [51], and Cicindelinae [80].
On the other hand, the shift in secretion composition may have a dietary origin, as observed
in species of the genus Scaphinotus [77]. These findings suggest the role of dietary chemical
precursors in the biosynthesis of chemical secretions.
Life 2021, 11, 562
9 of 22
Table 2. Components of pygidial gland secretions in Carabidae. Classification of taxa has been arranged according to Bousquet [56] and Beutel and Ribera [57].
Subfamily
Tribe
Genus
Species
Paussinae
Metriini
Metrius
M. contractus
Ozaeniini
Arthropterus
Mystropomus
Pachyteles
A. sp.
M. regularis
P. longicornis
P. striola
P. hirta
P. panamensis
H. arrawi
P. favieri
C. flexuosa
C. haemorrhagica
C. marutha
C. nigrocoerulea
C. punctulata chihuahuae
C. sedecimpunctata
C. sexguttata
C. abdominalis, C. andrewesi, C. angulata, C. assamensis,
C. aurofasciata, C. belfragei, C. bicolor, C. bigemina,
C. calligramma, C. cancellata, C. cardoni, C. catena,
C. celeripes, C. chloris, C. circumpicta, C. cuprascens,
C. depressula, C. duodecimguttata, C. duponti, C. erudita,
C. f. generosa, C. f. manitoba, C. fabriciana, C. fastidiosa,
C. fowleri, C. fulgida, C. grammophora, C. hamata,
C. hamiltoniana, C. hirticollis, C. horni, C. intermedia,
C. lemniscata, C. limbata, C. macra, C. melancholica,
C. minuta, C. motschulskyana, C. multiguttata, C. nevadica,
C. o. rectilatera, C. obsoleta, C. ocellata ocellata, C. oregona,
C. pamphila, C. pimeriana, C. pulchra, C. punctulata
punctulata, C. purpurea, C. repanda, C. rufiventris,
C. rugosiceps, C. s. lecontei, C. s. rugifrons, C. schauppi,
C. severa, C. severini, C. striatifrons, C. striolata,
C. sumatrensis, C. togata globicollis, C. tranquebarica,
C. venosa, C. virgula, C. westermanni, C. willistoni, C. lengi
O. annulicornis, O. cayennensis, O. confuse, O. luridipes
P. egregia
Paussini
Cicindelinae
Cicindelini
Physea
Platycerozaena
Homopterus
Paussus
Cicindela
Odontocheila
Pentacomia
Substances *
Refs
H18, H19, H20, H21, H22, H23, H25, H26, H27,
H28, H29, H36, H35, H37, H41, H42, H52, H53,
H54, H55, H56, H62, Q2, Q3, Q8, Q11, Q13
Q6, Q11
Q2, Q6, Q11
H52, Q2
H52, Q2
H52, Q2
H52, Q2, Q8, Q11
H52, Q2
Q2, Q11
E9, E19
A1, B1, E19, H52, H62
E9
E19
A1, E19
A1, T3
T3
[34]
[34]
[59]
[59]
[59]
[59]
[59]
[92]
[93]
[79]
[79]
[79]
[79]
[79]
[79]
A1
[79]
A1, H52
A1, H52
[79]
[79]
[62]
Life 2021, 11, 562
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Table 2. Cont.
Subfamily
Tribe
Genus
Species
Substances *
Refs
Cicindelinae
Collyridini
Megacephalini
Carabinae
Carabini
Neocollyris
Megacephala
Omus
Calosoma
N. variitarsus
M. carolina
O. audouini
C. (Campalita) chinense
C. externuum
C. marginalis
C. oceanicum
C. prominens
C. schayeri
C. sycophanta
C. auratus
C. auronitens
C. (Damastes) blaptoides
C. (Megodontus) caelatus
C. (Tachypus) cancellatus
C. cansellatus
C. cyaneus
C. (Tomogarabus) convexus
C. (Procustes) coriaceus
C. (Apotomopterus) dehaanii
C. granulatus
C. intricatus
C. (Platycarabus) irregularis
C. (Apotomopterus) japonicus
C. (Archicarabus) montivagus
C. porrecticollis
C. problematicus
C. procelus
C. taedutus
C. ullrichii
C. (M.) violaceus
C. (Apotomopterus) yaconinus
H. tuberculosus
A1
A1, B8, N1
B15
C4, F27, A2
C4
C4
A2, C4, F5
A2
A2, C4, F5
A2, C4, C5, B1, F2, F6, F11, F17, F25, F27
C4, F27
C4, F27
C2, C4, F27
B1, C1, C4, F1, F2, F8, F11, F17, F25, F27
C4, F27
C4, F27
C4, F27
B1, C4, F27
B1, C4, F27
C2, C4, F27
C4, F27
C4, F27
C4, F27
C2, C4, F27
C4, F27
C2, C4, F27
C4, F27
C2, C4, F27
C2, C4
B1, C4, F1, F2, F11, F17, F27
B1, C4, F1, F11, F17, F25, F27
C2, C4, F27
C2, C4
[79]
[79]
[79]
[33]
[28]
[28]
[34]
[30,64]
[34]
[30,48]
[28,30,78,94]
[30,78,94,95]
[33]
[43]
[30]
[78]
[30]
[30,42,78,94]
[30,42,49,94]
[33]
[30,78,94]
[94]
[30,94]
[33]
[43]
[33]
[28,78]
[30,33]
[67]
[30,49,94]
[30,43,94]
[33]
[33]
Carabus
Hemicarabus
Life 2021, 11, 562
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Table 2. Cont.
Subfamily
Tribe
Genus
Species
Substances *
Refs
Carabinae
Ceroglossini
Ceroglossus
Cychrini
Cychrus
Scaphinotus
Pamborus
Elaphrus
Loricera
Omophron
Leistus
Nebria
C. buqueti
C. chilensis
C. magellanicus
C. caraboides rostratus
S. andrewsi germari, S. andrewsi montana, S. virdus, S. webbi
P. alternans, P. guerini, P. pradieri, P. viridis
E. riparius
L. pilicornis
O. limbatum
L. ferrugineus
N. chinensis
N. lewisi
N. livida
N. macrogona
N. psammodes
N. biguttatus
N. impressifrons
S. aterrimus
S. subterraneus
S. cutidens
S. sulcatus
S. terricola
A. schaumii
C. basalis
C. fossor
S. puncticollis
S. lineolatus
D. wilsoni
P. subsulcatus
C. bonelli
C. interruptum
C. tinctillatum
L. foveigerum
P. tuberculatus
B. doenitzi
B1, C1, C2, C4, C5, F3, F11, F14, F27, H61, S1
B1, C2, C4, F3, F11, F14, F27, H61
B1, C2, C4, F3, F11, S1
C4, F27
C4, F27
C2, C4
F11, F14
F11, F14
F11, F14
C4, F27
C2, C4, F27
C2, C4, F27
C4, F27
C2, C4, F27
C4, F27
F11, F14
C4, F27
C4, F1, F6, F13, F27
C4, F1, F6, F11, F13, F27
C4, F1, F13, F27
C4, F1, F13, F27
C4, F1, F13, F27
Q11, T1, T4
Q1, Q11
Q1, Q6, Q2, Q11, Q12, Q13
Q2, Q11, T2, T4, T5, T6, T7
F8, F9, F10
B9, K2, K7, T3
C4, F1, F11, F14, F17, F25, F27
C4, F1, F7, F13
C4, F1, F13
C4, F1, F13, F27
C2, C4, F5, F6, F7, F13, F27
C4, F6, F12, F13, F27
F2, F14
[96]
[96]
[96]
[28,30,94]
[77]
[34]
[28]
[28]
[28]
[28,78]
[33]
[33]
[28,78]
[33]
[50]
[28]
[33]
[33]
[68]
[33]
[33]
[33]
[75]
[34]
[78]
[75]
[31]
[97]
[51,52]
[34]
[34]
[34]
[34]
[34]
[33]
Elaphrinae
Loricerinae
Omophroninae
Nebriinae
Pamborini
Elaphrini
Loricerini
Omophronini
Nebriini
Nebriinae
Notiophilini
Notiophilus
Scaritinae
Scaritini
Scarites
Clivinini
Ardistomis
Clivina
Broscinae
Dyschiriini
Pasimachini
Carenini
Semiardistomis
Schizogenius
Dyschirius
Pasimachus
Carenum
Broscini
Laccopterum
Philoscaphus
Broscosoma
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12 of 22
Table 2. Cont.
Subfamily
Trechinae
Tribe
Trechini
Bembidiini
Patrobinae
Patrobini
Genus
Species
Substances *
Refs
Broscus
Craspedonotus
Eurylychnus
Duvalius
B. cephalotes
C. tibialis
E. blagravei
E. ollifi
D. (Paraduvalius) milutini
[28,98,99]
[33]
[34]
[34]
[100]
Pheggomisetes
P. ninae
Trechoblemus
Bembidion
Calathus
Dolichus
T. postilenatus
B. lampros
B. lissonotum
B. morawitzi
B. quadriguttatum
B. semilunium
B. stenoderum
T. sericans
A. curtus
A. semilucidum
D. caligatus
D. depressus
P. flavipes
P. longicornis
M. simplex
M. seticollis
D. laevissimo
L. icarus
L. longiformis
L. velocipes
C. fuscipes
D. halensis
Laemostenus
L. punctatus
Synuchus
S. callitheres
S. cycloderus
S. dulcigradus
A. asperulus
A. anaea
F11, F14
F1, F11, F14
C4, F27
C4, F17, F27
B1, F4, F5, F15, F18, F22, F23, F24, F26
A1, C1, C5, F2, F11, F12, F14, F16, F18, F22, F23,
F26, H12, H16, H17, H24, H34, H38, H39, H40,
H45, H48, H49, H62, H65
F11, F14
F11, F14
C4, F27
C4, F27
A2, F28
C4, F27
C4, F27
F11, F14
C3
F2, F14
C4, F27
C4, F27
C4, F1, F13, F27
C1, C4, F27, K6
C1, C3, C4, F25, F27, H3, H4, H5, H6
B1, C1, C3, E6, E19, E20, E21, H3, H5, H6, H7
C1, C3, E1, E3, E4, E12, H1, H3
C1, C3, F7, H2, H3
A2
C1, C3, F7, H3, H7
C3
K8
C1, C3, E6, E20, F22, F23, F26, G2, H30, H32,
H65
C3
C3, K8
C3, K8
C3, C4, F1, F27
C4, F27, H3, H4, H5
Tachys
Amblytelus
Asaphidion
Diplous
Patrobus
Harpalinae
Morionini
Perigonini
Loxandrini
Sphodrini
Pterostichini
Morion
Moriosomus
Diploharpus
Loxandrus
Abacomorphus
Abaris
[100]
[33]
[28]
[33]
[33]
[78]
[33]
[33]
[33]
[34]
[33]
[33]
[33]
[33]
[31]
[31]
[31]
[31]
[31]
[34]
[31]
[98,99]
[101]
[87,100]
[33]
[33]
[33,101]
[34]
[31]
Life 2021, 11, 562
13 of 22
Table 2. Cont.
Subfamily
Tribe
Genus
Species
Substances *
Refs
Blennidus
Castelnaudia
Cratoferonia
Cratogaster
Cyclotrachelus
Gasterllarius
Incastichus
Lesticus
Loxodactylus
Myas
B. liodes
C. superba
C. phylarchus
C. melas
C. sigillatus
G. honestus
I. aequidianus
L. magnus
L. carinulatus
M. coracinus
N. angustibasis, N. crenulatus, N. miles, N. muelleri, N.
opulentus, N. rainbowi, N. scotti, N. triplogenioides, N.
variicollis
P. coerulescens
P. cupreus
P. fortipes
P. harpaloides
P. iridescens
P. (Hypherpes) californicus
P. (Cophosus) cylindricus
P. daisenicus
P. (Monoferonia) diligendus
P. externepunctatus roccai
P. fortis
P. fujimurai
P. longinquus
P. luctuosus
P. macer
P. masidai
P. (Ferodinius) melas
P. metallicus
P. microcephalus
P. niger
C4, F14, F27, H4
C1, C4, F27
C4, F27
C4, F27
C1, C3
C4, F25
C1, C3
C4, F27
C3
C4, F25, F27
[31]
[34]
[34]
[34]
[31]
[31]
[31]
[33]
[34]
[31]
C3
[34]
C4, F27
C4, F27, H8, H62, H65
C4, F27
C4
C4, F27
C2, F17, F27
C4, F27
C2, C4, F27
C4, F27
C4, F11, F27, H62, H65
C2, C4, F27
C2, C4, F27
C2, C4, F27
C4, F27
C4, F27, H8, H62, H65
C2, C4, F27
C4, F11, F17, F25, F27, H8, H62, H65
C4, F27, H8, H62, H65
C2, C4, F27
C4, F27, H8, H62, H65
C1, C4, C5, F9, F11, F17, F27, H13, H14, H15,
H57, H60, H62, H64, H65
C2, C4, F27
C2, C4, F27
[33]
[78]
[33]
[34]
[34]
[69]
[44]
[33]
[31]
[50]
[33]
[33]
[33]
[31]
[28,78]
[33]
[28,44,78]
[28,30,78,94]
[33]
[28,30,78,94]
Notonomus
Poecilus
Prosopogmus
Pseudoceneus
Pterostichus
P. (Pseudomaseus) nigrita
P. prolongatus
P. rotundangulus
[44]
[33]
[33]
Life 2021, 11, 562
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Table 2. Cont.
Subfamily
Tribe
Genus
Platynini
Rhytisternus
Sarticus
Sphodrosomus
Trichosternus
Trigonotoma
Trigonognatha
Agonum
Anchomenus
Colpodes
Loxocrepis
Lorostemma
Platynus
Zabrini
Amara
Molopini
Bradytus
Curtonotus
Abax
Molops
Harpalini
Anisodactylus
Anoplogenius
Bradycellus
Diaphoromerus
Harpalus
Species
Substances *
Refs
P. vulgaris
R. laevilaterus
S. cyaneocinctus
S. saisseri
T. nudipes
T. lewisii
T. cuprescens
A. chalcomum
A. daimio
A. (Idiochroma) dorsalis
A. leucopus
C. atricomes
C. japonicus
L. rubriola
L. ogurae
P. brunneomarginatus
P. magnus
P. ovipennis
P. protensus
A. chalcites
A. chalcophaea
A. familiaris
A. similata
B. ampliatus, B. simplicidens
C. giganteus
A. ovalis
A. parallelepipedus (sub:A. ater)
A. parallelus
M. elatus
M. (Stenochoromus) montenegrinus
A. signatus
A. tricuspidatus
A. cyanescens
B. inornatus
D. edwardsi
H. atratus
H. capito
C4, F27, H8, H62, H65
C4, F27
C3
C3
C4, F27
C4, F27
C4, F27
C3, K8
C3
H14, H58, H60, H65
C3
C3
C3
C3
C3
C3, F18, F23, H52, H62, H65, K1, K3, K6, K8
C3
C3, F19, H52, H62, H65, K1, K3, K6, K8
C3, K8
C2, C4, F1, F27
C2, C4, F1, F27
C4, F27, H8, H62, H65
C4, F27, H8, H62, H65
C2, C4, F1, F27
C2, C4, F1, F27
C4, F27
C4, C5, F6, F11, F25, F27
C4, F27
C4, F27
C1, C4, C5, F1, F2, F5, F8, F9, F11, F17, F28
C3, K8
C3
C3
C3
C3
C3
C3, K8
[30,78,94]
[34]
[34]
[34]
[34]
[33]
[33]
[33,101]
[33]
[28]
[33]
[33]
[33]
[33]
[33]
[31]
[33]
[102]
[33,101]
[33]
[33]
[28,78]
[28,78]
[33]
[33]
[28,30,78]
[28,30,49,78]
[30,78,95]
[28,78]
[44]
[33,101]
[33]
[33]
[33]
[34]
[98,99]
[33,101]
Life 2021, 11, 562
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Table 2. Cont.
Subfamily
Tribe
Genus
Platymetopus
Pseudophonus
Stenolophus
Licinini
Trichocellus
Trichotichnus
Dicrochile
Diplocheila
Chlaeniini
Syagonix
Callistoides
Callistus
Chlaenius
Epomis
Macrochlaenites
Oodes
Species
Substances *
Refs
H. dimidiatus
H. distinguendus
H. luteicornis
H. platynotus
H. sinicus
H. tardus
P. flavibarbis
P. griseus
P. rufipes (sub:pubescens)
S. agonoides
S. difficilis
S. iridicolor
T. tenuimanus
T. longitarsis
D. brevicollis
D. goryi
D. elongata
D. zeelandica
S. blackburni
C. delciolus
C. lunatus
C. basalis
C. australis
C. circumdatus
C. cordicollis
C. (Chlaeniellus) inops
C. noguchii
C. pallipes
C. (Chlaeniellus) postemus
C. spoliatus
C. velutinus
C. vestitus
C. virgulifer
E. nigricans
M. costiger
O. amaroides
C3
C3
C3
C3
C3
C3
C3
C3
C3
C3, H63
C3
C3
C3
C3, H63
C3
C3
C3
C3, H63
C3
B2
Q2, Q11
Q2
B2
B2
B2, B4, B3, B5, B7, B11, B12
Q1, Q6, Q10
B2
B2
Q1, Q6, Q10
B2
B2, B4, B6, H22, H52, Q1, Q7, Q11
B2, Q2
B2
B2
B2
A2, B1, C1, F11, F14
[30]
[98,99]
[98,99]
[33]
[33]
[98,99]
[33]
[30,33,94]
[30,94]
[33,101]
[33]
[33]
[33]
[33,101]
[34]
[34]
[33]
[33,101]
[34]
[33]
[28]
[28]
[34]
[33]
[30,91]
[33]
[33]
[33]
[33]
[33]
[50]
[28,50]
[33]
[33]
[33]
[31]
Life 2021, 11, 562
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Table 2. Cont.
Subfamily
Tribe
Genus
Species
O. americanus
Panagaenini
Dischissus
Panagaeus
Cymindis
Dolichoctis
D. mirandus
P. bipustulatus
P. japonicus
P. auripilis
P. nigrinus
A. bimaculata nipponica
C. pensylvanica
O. melanura
A. grandis
C. lepida
L. retrofasciata
E. macleayi
C. japonica
C. subapicalis
C. daimio
D. striatus
Helluomorphoides
H. clairvillei
Lebidia
H. ferrugineus
H. latitarsis
L. octoguttata
Galerita
G. lecontei
Galeritula
Planetes
Anthia
Thermophilum
G. japonica
P. puncticeps
A. thoracica
T. burchelli
T. homoplatum
H. costatus
C. attenuata
C. sulcipennis
D. japonica
S. colymbeioides
Peronomerus
Odacanthini
Lebiini
Galeritini
Anthiini
Archiocolliuris
Colliuris
Odacantha
Apristus
Callida
Lebia
Eudalia
Coptodera
Helluonini
Catapieseini
Helluo
Catapiesis
Dryptini
Pseudomorphini
Drypta
Sphallomorpha
Substances *
B1, C1, C4, C5, F11, F2, F5, F6, F8, F14, F17, F21,
F27
B2
B2
B2
B2
B2
H63
C1, C3, H3, K6
C3
C3, H63
C3
C3
C3
C3
C3
H63
C3, H63
H43, H9, H8, H65, E8, H11, E17, E14, E16, E12,
E3, E15, E1, E21, E3, E22, E13, E5, E20, E7, E6,
H14, H31, H58, H33
C3, E12
C3, E12
C3, H63
C3, E1, E2, E3, E5, E6, E13, E12, E17, E20, G1, H8,
H43, H44, H46, H62, H65, H66, H67
C3, E1, E3, E12
C3, E1, E3, E12
A3, C1, C3, F1, F27
C1, C3, F1, F27
A3, C1, C3, F1, F27
C3, E12, E13
C3, E1, H1, H3
E1
C3, E1, E3, E12
C3
Refs
[89]
[33]
[98,99]
[33]
[33]
[33]
[101]
[31]
[28]
[33,101]
[33]
[33]
[34]
[33]
[33]
[101]
[33,101]
[85]
[84]
[84]
[33,101]
[45]
[33,101]
[33,101]
[103]
[103]
[103]
[34]
[31]
[31]
[33,101]
[34]
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Table 2. Cont.
Subfamily
Tribe
Genus
Species
Substances *
Refs
Brachininae
Brachinini
Brachinus
B. chuji
B. crepitans
B. elongatus
B. explodens
B. sclopeta
B. scotomedes
B. stenoderus
P. africanus
P. agnatus
P. catoirei
P. verticalis
P. jessoensis
Q1, Q9
Q2, Q11
H10, H14, H60, Q2, Q4, Q5, Q8, Q11, Q12
Q2, Q11
Q2, Q11
Q1, Q9
Q1, Q9
N2, N3
C3
Q2, Q11
Q1, Q11
Q1, Q9
[33]
[28,30]
[41,55,66]
[28,30]
[30,41]
[33]
[33]
[30,41]
[30]
[104]
[34]
[33]
Pheropsophus
* Abbreviations [Aldehydes (A)—A1: benzaldehyde; A2: salicylaldehyde; A3: iso-valeraldehyde. Benzene, substituted derivatives and phenols (B)—B1: benzoic acid; B2: cresols, (m-cresol), (3-methylphenol);
B3: 2,3-dimethylphenol; B4: 2,5-dimethylphenol; B5: 3,4-dimethylphenol; B6: 3,5-dimethylphenol; B7: 3-ethylphenol; B8: mandelonitril; B9: methyl 2-hydroxy-6-methylbenzoate; B10: methyl salicylate;
B11: 2-methoxy-5-methylphenol; B12: 2-methoxy-4-m-cresol; B13: 2-phenylethanol; B14: 2-phenylethyl; B15: phenylacetic acid; B16: xylenol isomer. Carboxylic acids and derivatives (C)—C1: acetic acid;
C2: ethacrylic acid; C3: formic acid; C4: methacrylic acid; C5: propanoic acid (propionic acid). Fatty alcohol esters (E)—E1: decyl acetate; E2: decyl butyrate; E3: decyl formate; E4: decyl hexanoate; E5: decyl
propionate; E6: dodecyl acetate; E7: dodecyl formate; E8: heptyl acetate; E9: hexadecyl acetate; E10: isopropyl ethacrylate; E11: isopropyl methacrylate; E12: nonyl acetate; E13: nonyl butyrate; E14: nonyl
formate; E15: nonyl propionate; E16: 3-nonen-l-yl acetate; E17: octyl acetate; E18: 2-phenylethyl ethacrylate; E19: tetradecyl acetate; E20: undecyl acetate; E21: undecyl formate; E22: 4-undecen-l-yl acetate.
Fatty acids and conjugates (F)—F1: angelic acid; F2: butyric acid; F3: n-butanoic acid; F4: capric acid; F5: caproic acid (hexanoic acid); F6: crotonic acid; F7: hexenoic acid; F8: 2-hexenoic acid; F9: 3-hexenoic
acid; F10: 3,5-hexadienoic; F11: isobutyric acid; F12: isocaproic acid; F13: isocrotonic acid; F14: isovaleric acid (3-methylbutyric acid); F15: lauric acid; F16: linoleic acid; F17: 2-methylbutyric acid; F18: myristic
acid; F19: nonanoic acid; F20: octanoic acid (caprylic acid); F21: 2-octenoic acid; F22: oleic acid; F23: palmitic acid; F24: pelargonic acid; F25: senecioic acid; F26: stearic acid; F27: tiglic acid; F28: valeric acid.
Fatty alcohol (G)—G1: 1-decanol; G2: dodecan-1-ol. Hydrocarbons (H)—H1: C9:0; H2: C10:0; H3: C11:0; H4: C12:0; H5: C13:0; H6: C15:0; H7: C17:0; H8: decane; H9: 1-decene + 3-decene; H10: 9-docosene;
H11: dodecane; H12: 3-ethyltetracosane; H13: heneicosadiene; H14: heneicosane; H15: heneicosene; H16: heptacosadiene; H17: heptacosene; H18: 5,7-heptadecadiene; H19: 7,9-heptadecadiene; H20: (6Z,9Z)6,9-heptadecadiene; H21: (7Z,9Z)-7,9-heptadecadiene; H22: heptadecane; H23: (Z)-8-heptadecene; H24: hexacosane; H25: hexadecadiene; H26: 6,8-hexadecadiene; H27: 7,9-hexadecadiene; H28: hexadecane;
H29: hexadecene; H30: 7-hexyldocosane; H31: 9-methylheneicosane; H32: 9-methyltetracosane; H33: 9-methyltricosane; H34: 11-methylheptacosane; H35: 3-methylpentadecane; H36: 4-methylpentadecane;
H37: 5-methylpentadecane; H38: nonacosapentaene; H39: nonacosatetraene; H40: nonacosene; H41: nonadecane; H42: 7,9-nonadecadiene; H43: nonane; H44: 1-nonene; H45: octacosane; H46: octane;
H47: pentacosadiene; H48: pentacosane; H49: pentacosene; H50: (Z)-7-pentacosene; H51: (Z)-9-pentacosene; H52: pentadecane; H53: 5,7-pentadecadiene; H54: 6,8-pentadecadiene; H55: 7-pentadecene;
H56: tetradecane; H57: tricosadiene; H58: tricosane; H59: (Z)-7-tricosene; H60: (Z)-9-tricosene; H61: 11-tricosene; H62: tridecane; H63: 2-tridecane; H64: tricosatriene; H65: undecane; H66: 4-undecene;
H67: 5-undecene. Ketone (K)—K1: 2-dodecanone; K2: 2-heptanone; K3: 2-heptadecanone; K4: 2-hexanone; K5: 3-hexanone; K6: 2-pentadecanone; K7: 2-pentanone; K8: 2-tridecanone. Non-metal
oxoanionic compounds and organonitrogen compounds (N)—N1: hydrogen cyanide; N2: nitrites; N3: nitrous acid. Quinone (Q)—Q1: benzoquinone; Q2: 1,4-benzoquinone; Q3: 2-chloro-1,4-benzoquinone;
Q4: 2,5-dimethyl-1,4-benzoquinone; Q5: 2,3-dimethyl-1,4-benzoquinone; Q6: 2-ethylquinone; Q7: ethylbenzoquinone; Q8: 2-ethyl-1,4-benzoquinone; Q9: 2-methylbenzoquinone; Q10: 2-methylquinone;
Q11: 2-methyl-1,4-benzoquinone (toluquinone); Q12: methoxy-1,4-benzoquinone; Q13: 2-methoxy-3-methyl-1,4-benzoquinone. Terpenes (T)—T1: 1,8-cineole; T2: p-cymene; T3: iridodial; T4: (R)-(+)-limonene,
(S)-(-)-limonene; T5: sabinene; T6: β-phellandrene; T7: β-pinene. Thioethers (S)—S1: 3-methyl-1-(methylthio)-2-butene.].
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5. Concluding Remarks
Pygidial glands are homologous structures in the Carabidae. They show a range of
morphological variations in structural elements, i.e., number of acini, the morphology of
ducts and reservoir chamber, and mode of secretion discharge, among carabid species,
regardless of habitat and associated ecological differences. Chemical defences are an important part of antipredator strategies in ground beetles. Prey–predator coevolution likely
influences glandular secretion composition, which is the result of a trade-off between the
predator diversity and the fitness costs of defending against these enemies. A great deal of
interspecific diversity in the distribution of substances has been found in subfamilies. Some
chemicals are readily identifiable as specific to particular taxa, while others show great
species-level diversity among genera or tribes. These results are broadly consistent with
previous studies in which the taxonomic distribution of compound secretion was reviewed
according to habitat diversification and by mapping chemical classes in a phylogenetic
context [31,33]. However, some elements need to be considered in the future interpretation
of the taxonomic distribution of chemicals. The findings pertain to only the 4% of carabid
species so far described, and further studies are needed to clarify differences in chemical
composition in additional taxa. A large number of studies reported only the most abundant chemicals, neglecting compounds that are present in smaller percentages and have
additional biological functions in the mixture, e.g., surfactants, pheromones, and antiseptic
agents. In addition, the differences found in some chemical profiles may be related to the
number of samples analysed as single or mixed samples or to the accuracy of the gas chromatographic equipment used in early studies. Finally, we recommend that further research
should address to elucidate: (1) the biogenesis of all chemicals described in the pygidial
glands and their function in an ecological context; (2) clarify the phylogenetic distribution
patterns of chemicals by studying as many species as possible using comparable protocols;
(3) the sexual dimorphism of the secretion with regard to the different degree of resource
allocation between the sexes under the pressure of environmental selection.
Author Contributions: Conceptualisation, A.G.; data curation, F.T. and M.L.V.; validation of taxonomy, P.B.; writing—original draft preparation, A.G.; writing—review and editing: A.G., M.L.V. and
F.T. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: No new data were created or analyzed in this study. Data sharing is
not applicable to this article.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or
in the decision to publish the results.
References
1.
2.
3.
4.
5.
6.
7.
Holland, J.M. The Agroecology of Carabid Beetles; Intercept Limited: Andover, UK, 2002; Volume 62, ISBN 1898298769.
Lövei, G.L.; Sunderland, K.D. Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu. Rev. Entomol. 1996,
41, 231–256. [CrossRef] [PubMed]
Koivula, M.J. Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental
conditions. ZooKeys 2011, 287–317. [CrossRef] [PubMed]
Rainio, J.; Niemelä, J. Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodivers. Conserv. 2003, 12, 487–506. [CrossRef]
Avgın, S.S.; Luff, M.L. Ground beetles (Coleoptera: Carabidae) as bioindicators of human impact. Munis Entomol. Zool. 2010,
5, 209–215.
Ghannem, S.; Touaylia, S.; Boumaiza, M. Beetles (Insecta: Coleoptera) as bioindicators of the assessment of environmental
pollution. Hum. Ecol. Risk Assess. Int. J. 2018, 24, 456–464. [CrossRef]
Tooming, E.; Merivee, E.; Must, A.; Merivee, M.-I.; Sibul, I.; Nurme, K.; Williams, I.H. Behavioural effects of the neonicotinoid
insecticide thiamethoxam on the predatory insect Platynus assimilis. Ecotoxicology 2017, 26, 902–913. [CrossRef]
Life 2021, 11, 562
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
19 of 22
Giglio, A.; Cavaliere, F.; Giulianini, P.G.; Kurtz, J.; Vommaro, M.L.; Brandmayr, P. Continuous agrochemical treatments in
agroecosystems can modify the effects of pendimethalin-based herbicide exposure on immunocompetence of a beneficial ground
beetle. Diversity 2019, 11, 241. [CrossRef]
Butovsky, R.O. Heavy metals in carabids (Coleoptera, Carabidae). ZooKeys 2011, 100, 215–222. [CrossRef]
Talarico, F.; Brandmayr, P.; Giulianini, P.G.; Ietto, F.; Naccarato, A.; Perrotta, E.; Tagarelli, A.; Giglio, A. Effects of metal pollution
on survival and physiological responses in Carabus (Chaetocarabus) lefebvrei (Coleoptera, Carabidae). Eur. J. Soil Biol. 2014,
61, 80–89. [CrossRef]
Tőzsér, D.; Magura, T.; Simon, E.; Mizser, S.; Papp, D.; Tóthmérész, B. Pollution intensity-dependent metal accumulation in
ground beetles: A meta-analysis. Environ. Sci. Pollut. Res. 2019, 26, 32092–32102. [CrossRef]
Naccarato, A.; Tassone, A.; Cavaliere, F.; Elliani, R.; Pirrone, N.; Sprovieri, F.; Tagarelli, A.; Giglio, A. Agrochemical treatments as
a source of heavy metals and rare earth elements in agricultural soils and bioaccumulation in ground beetles. Sci. Total Environ.
2020, 749, 141438. [CrossRef]
Giglio, A.; Brandmayr, P. Structural and functional alterations in Malpighian tubules as biomarkers of environmental pollution:
Synopsis and prospective. J. Appl. Toxicol. 2017, 37, 889–894. [CrossRef] [PubMed]
De Heij, S.E.; Willenborg, C.J. Connected carabids: Network interactions and their impact on biocontrol by carabid beetles.
BioScience 2020, 70, 490–500. [CrossRef] [PubMed]
Kulkarni, S.S.; Dosdall, L.M.; Willenborg, C.J. The role of ground beetles (Coleoptera: Carabidae) in weed seed consumption: A
review. Weed Sci. 2015, 63, 355–376. [CrossRef]
Fukuda, S.; Konuma, J. Using three-dimensional printed models to test for aposematism in a carabid beetle. Biol. J. Linn. Soc.
2019, 128, 735–741. [CrossRef]
Schultz, T.D. Tiger beetle defenses revisited: Alternative defense strategies and colorations of two neotropical tiger beetles,
Odontocheila nicaraguensis Bates and Pseudoxycheila tarsalis Bates (Carabidae: Cicindelinae). Coleopt. Bull. 2001, 153–163. [CrossRef]
Hasegawa, M.; Taniguchi, Y. Visual avoidance of a conspicuously colored carabid beetle Dischissus mirandus by the lizard
Eumeces okadae. J. Ethol. 1994, 12, 9–14. [CrossRef]
Brandmayr, P.; Bonacci, T.; Giglio, A.; Talarico, F.F.; Brandmayr, T.Z. The evolution of defence mechanisms in carabid beetles: A
review. In Life and Time: The Evolution of Life and its History; Cleup: Padova, Italy, 2009; pp. 25–43. ISBN 9788861294110.
Talarico, F.; Brandmayr, P.; Giglio, A.; Massolo, A.; Brandmayr, T.Z. Morphometry of eyes, antennae and wings in three species of
Siagona (Coleoptera, Carabidae). ZooKeys 2011, 100, 203–214. [CrossRef]
Whitman, D.W.; Blum, M.S.; Alsop, D.W. Allomones: Chemicals for defense. Insect Def. Adapt. Mech. Strateg. Prey Predat. 1990,
289, 289–351.
Dettner, K. Chemosystematics and evolution of beetle chemical defenses. Annu. Rev. Entomol. 1987, 32, 17–48. [CrossRef]
Giglio, A.; Brandmayr, P.; Talarico, F.; Brandmayr, T.Z. Current knowledge on exocrine glands in carabid beetles: Structure,
function and chemical compounds. ZooKeys 2011, 100, 193–201. [CrossRef]
Evans, D.L.; Schmidt, J.O. Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators; SUNY Press: Albany, NY, USA,
1990; ISBN 1438402201.
Blum, M.S. Semiochemical parsimony in the Arthropoda. Annu. Rev. Entomol. 1996, 41, 353–374. [CrossRef]
Lečić, S.; Ćurčić, S.; Vujisić, L.; Ćurčić, B.; Ćurčić, N.; Nikolić, Z.; Anelković, B.; Milosavljević, S.; Tešević, V.; Makarov, S. Defensive
secretions in three ground-beetle species (Insecta: Coleoptera: Carabidae). Proc. Ann. Zool. Fenn. 2014, 51, 285–300. [CrossRef]
Rork, A.M.; Renner, T. Carabidae semiochemistry: Current and future directions. J. Chem. Ecol. 2018, 44, 1069–1083. [CrossRef]
[PubMed]
Blum, M. Chemical defenses of Arthropods. In Chemical Defenses of Arthropods; Blum, M.S., Ed.; Academic Press: New York, NY,
USA, 1981; p. 561. ISBN 978-0-12-108380-9.
Erwin, T.L.; Ball, G.E.; Whitehead, D.R.; Halpern, A.L. Carabid Beetles: Their Evolution, Natural History, and Classification; Springer
Science & Business Media: Dordrecht, The Netherlands, 2012; ISBN 9400996284.
Dazzini-Valcurone, M.; Pavan, M. Glandole pigidiali e secrezioni difensive dei Carabidae (Insecta Coleoptera). Publicazioni
Dell’istituto Di Entomol. Dell’universita Di Pavia 1980, 12, 1–36.
Will, K.W.; Attygalle, A.B.; Herath, K. New defensive chemical data for ground beetles (Coleoptera: Carabidae): Interpretations
in a phylogenetic framework. Biol. J. Linn. Soc. 2000, 71, 459–481. [CrossRef]
Moore, B.P. Chemical defense in carabids and its bearing on phylogeny. In Carabid Beetles; Springer: Dordrecht, The Netherlands,
1979; pp. 193–203.
Kanehisa, K.; Murase, M. Comparative study of the pygidial defensive systems of carabid beetles. Appl. Entomol. Zool. 1977,
12, 225–235. [CrossRef]
Moore, B.P.; Wallbank, B.E. Chemical composition of the defensive secretion in carabid beetles and its importance as a taxonomic
character. In Proceedings of the Royal Entomological Society of London. Series B, Taxonomy; Wiley Online Library: Oxford, UK, 1968;
Volume 37, pp. 62–72.
Forsyth, D.J. The structure of the pygidial defence glands of Carabidae (Coleoptera). Trans. Zool. Soc. Lond. 1972, 32, 249–309.
[CrossRef]
Noirot, C.; Quennedey, A. Fine Structure of Insect Epidermal Glands. Annu. Rev. Entomol. 1974, 19, 61–80. [CrossRef]
Life 2021, 11, 562
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
59.
60.
61.
62.
63.
20 of 22
Noirot, C.; Quennedey, A. Glands, gland cells, glandular units: Some comments on terminology and classification. In Annales De
La Societe Entomologique De France; Société entomologique de France: Paris, France, 1991; Volume 27, pp. 123–128.
Forsyth, D.J. The ultrastructure of the pygidial defence glands of the carabid Pterostichus madidus F. J. Morphol. 1970, 131, 397–415.
[CrossRef]
Muzzi, M.; Moore, W.; Di Giulio, A. Morpho-functional analysis of the explosive defensive system of basal bombardier beetles
(Carabidae: Paussinae: Metriini). Micron 2019, 119, 24–38. [CrossRef] [PubMed]
Muzzi, M.; Di Giulio, A. The ant nest “bomber”: Explosive defensive system of the flanged bombardier beetle Paussus favieri
(Coleoptera, Carabidae). Arthropod Struct. Dev. 2019, 50, 24–42. [CrossRef]
Di Giulio, A.; Muzzi, M.; Romani, R. Functional anatomy of the explosive defensive system of bombardier beetles (Coleoptera,
Carabidae, Brachininae). Arthropod Struct. Dev. 2015, 44, 468–490. [CrossRef] [PubMed]
Vesović, N.; Vujisić, L.; Perić-Mataruga, V.; Krstić, G.; Nenadić, M.; Cvetković, M.; Ilijin, L.; Stanković, J.; Ćurčić, S. Chemical
secretion and morpho-histology of the pygidial glands in two Palaearctic predatory ground beetle species: Carabus (Tomocarabus)
convexus and C. (Procrustes) coriaceus (Coleoptera: Carabidae). J. Nat. Hist. 2017, 51, 545–560. [CrossRef]
Vesović, N.; Ćurčić, S.; Todosijević, M.; Nenadić, M.; Zhang, W.; Vujisić, L. Pygidial gland secretions of Carabus Linnaeus, 1758
(Coleoptera: Carabidae): Chemicals released by three species. Chemoecology 2020, 30, 59–68. [CrossRef]
Vranić, S.; Ćurčić, S.; Vesović, N.; Mandić, B.; Pantelić, D.; Vasović, M.; Lazović, V.; Zhang, W.; Vujisić, L. Chemistry and
morphology of the pygidial glands in four Pterostichini ground beetle taxa (Coleoptera: Carabidae: Pterostichinae). Zoology 2020,
142, 125772. [CrossRef]
Rossini, C.; Attygalle, A.B.; González, A.; Smedley, S.R.; Eisner, M.; Meinwald, J.; Eisner, T. Defensive production of formic acid
(80%) by a carabid beetle (Galerita lecontei). Proc. Natl. Acad. Sci. USA 1997, 94, 6792–6797. [CrossRef]
Deuve, T. L’abdomen et les genitalia des femelles de Coleopteres Adephaga. Mem. Du Mus. Natl. D’histoire Nat. Paris 1993,
155, 1–184.
Forsyth, D.J. The structure of the defence glands of the Cicindelidae, Amphizoidae, and Hygrobiidae (Insecta: Coleoptera). J.
Zool. 1970, 160, 51–69. [CrossRef]
Nenadić, M.; Soković, M.; Glamočlija, J.; Ćirić, A.; Perić-Mataruga, V.; Ilijin, L.; Tešević, V.; Todosijević, M.; Vujisić, L.; Vesović, N.;
et al. The pygidial gland secretion of the forest caterpillar hunter, Calosoma (Calosoma) sycophanta: The antimicrobial properties
against human pathogens. Appl. Microbiol. Biotechnol. 2017, 101, 977–985. [CrossRef]
Nenadić, M.; Soković, M.; Glamočlija, J.; Ćirić, A.; Perić-Mataruga, V.; Ilijin, L.; Tešević, V.; Vujisić, L.; Todosijević, M.; Vesović, N.
Antimicrobial activity of the pygidial gland secretion of three ground beetle species (Insecta: Coleoptera: Carabidae). Sci. Nat.
2016, 103, 34. [CrossRef]
Balestrazzi, E.; Valcurone Dazzini, M.L.; De Bernardi, M.; Vidari, G.; Vita-Finzi, P.; Mellerio, G. Morphological and chemical
studies on the pygidial defence glands of some Carabidae (Coleoptera). Naturwissenschaften 1985, 72, 482–484. [CrossRef]
Davidson, B.S.; Eisner, T.; Witz, B.; Meinwald, J. Defensive secretion of the carabid beetle Pasimachus subsulcatus. J. Chem. Ecol.
1989, 15, 1689–1697. [CrossRef]
Witz, B.W.; Mushinsky, H.R. Pygidial secretions of Pasimachus subsulcatus (Coleoptera: Carabidae) deter predation by Eumeces
inexpectatus (Squamata: Scincidae). J. Chem. Ecol. 1989, 15, 1033–1044. [CrossRef] [PubMed]
Donato, S.; Vommaro, M.L.; Tromba, G.; Giglio, A. Synchrotron X-ray phase contrast micro tomography to explore the morphology
of abdominal organs in Pterostichus melas italicus Dejean, 1828 (Coleoptera, Carabidae). Arthropod Struct. Dev. 2021, 62, 101044.
[CrossRef]
Rork, A.M.; Mikó, I.; Renner, T. Pygidial glands of Harpalus pensylvanicus (Coleoptera: Carabidae) contain resilin-rich structures.
Arthropod Struct. Dev. 2019, 49, 19–25. [CrossRef]
Arndt, E.M.; Moore, W.; Lee, W.K.; Ortiz, C. Mechanistic origins of Bombardier beetle (Brachinini) explosion-induced defensive
spray pulsation. Science 2015, 348, 563–567. [CrossRef]
Bousquet, Y. Catalogue of Geadephaga (Coleoptera, Adephaga) of America, north of Mexico. ZooKeys 2012, 1–1630. [CrossRef]
[PubMed]
Beutel, R.G.; Ribera, I.; Fikáček, M.; Vasilikopoulos, A.; Misof, B.; Balke, M. The morphological evolution of the Adephaga
(Coleoptera). Syst. Entomol. 2020, 45, 378–395. [CrossRef]
Thiele, H.-U. Carabid Beetles in Their Environments: A Study on Habitat Selection by Adaptations in Physiology and Behaviour; Springer
Science & Business Media: Dordrecht, The Netherland, 1977; Volume 10, ISBN 364281154X.
Roach, B.; Dodge, K.R.; Aneshansley, D.J.; Wiemer, D.; Meinwald, J.; Eisner, T. Chemistry of defensive secretions of Ozaenine and
Paussine bombardier beetles (Coleoptera: Carabidae). Coleopt. Bull. 1979, 33, 17–20.
Aneshansley, D.J.; Eisner, T.; Widom, J.M.; Widom, B. Biochemistry at 100 ◦ C: Explosive secretory discharge of bombardier beetles
(Brachinus). Science 1969, 165, 61–63. [CrossRef]
Eisner, T.; Aneshansley, D.J. Spray aiming in the bombardier beetle: Photographic evidence. Proc. Natl. Acad. Sci. USA 1999, 96,
9705–9709. [CrossRef]
Eisner, T.; Aneshansley, D.J.; Eisner, M.; Attygalle, A.B.; Alsop, D.W.; Meinwald, J. Spray mechanism of the most primitive
bombardier beetle (Metrius contractus). J. Exp. Biol. 2000, 203, 1265–1275. [CrossRef]
Eisner, T.; Aneshansley, D.J. Spray aiming in bombardier beetles: Jet deflection by the coanda effect. Science 1982, 215, 83–85.
[CrossRef]
Life 2021, 11, 562
64.
65.
66.
67.
68.
69.
70.
71.
72.
73.
74.
75.
76.
77.
78.
79.
80.
81.
82.
83.
84.
85.
86.
87.
88.
89.
90.
91.
92.
93.
94.
21 of 22
Eisner, T.; Swithenbank, C.; Meinwald, J. Defense Mechanisms of Arthropods. VIII. Secretion of salicylaldehyde by a carabid
beetle. Ann. Entomol. Soc. Am. 1963, 56, 37–41. [CrossRef]
Blum, M.S. Biosynthesis of arthropod exocrine compounds. Annu. Rev. Entomol. 1987, 32, 381–413. [CrossRef]
Attygalle, A.B.; Xu, S.; Moore, W.; McManus, R.; Gill, A.; Will, K. Biosynthetic origin of benzoquinones in the explosive discharge
of the bombardier beetle Brachinus elongatulus. Sci. Nat. 2020, 107, 1–11. [CrossRef] [PubMed]
Benn, M.H.; Lencucha, A.; Maxie, S.; Telang, S.A. The pygidial defensive secretion of Carabus taedatus. J. Insect Physiol. 1973,
19, 2173–2176. [CrossRef]
Attygalle, A.B.; Meinwald, J.; Eisner, T. Biosynthesis of methacrylic acid and isobutyric acids in a carabid beetle, Scarites
subterraneus. Tetrahedron Lett. 1991, 32, 4849–4852. [CrossRef]
Attygalle, A.B.; Wu, X.; Will, K.W. Biosynthesis of tiglic, ethacrylic, and 2-methylbutyric acids in a carabid beetle, Pterostichus
(Hypherpes) Californicus. J. Chem. Ecol. 2007, 33, 963–970. [CrossRef] [PubMed]
Chapman, R.F. The Insects: Structure and Function; Cambridge University Press: Cambridge, UK, 2012; ISBN 1107310458.
Pasteels, J.M.; Gregoire, J.C.; Rowell-Rahier, M. The chemical ecology of defense in arthropods. Annu. Rev. Entomol. 1983,
28, 263–289. [CrossRef]
Kojima, W.; Yamamoto, R. Defense of bombardier beetles against avian predators. Sci. Nat. 2020, 107, 1–5. [CrossRef]
Sugiura, S. Anti-predator defences of a bombardier beetle: Is bombing essential for successful escape from frogs? PeerJ 2018,
2018, e5942. [CrossRef] [PubMed]
Geiselhardt, S.F.; Peschke, K.; Nagel, P. A review of myrmecophily in ant nest beetles (Coleoptera: Carabidae: Paussinae): Linking
early observations with recent findings. Naturwissenschaften 2007, 94, 871–894. [CrossRef]
Attygalle, A.B.; Wu, X.; Maddison, D.R.; Will, K.W. Orange/lemon-scented beetles: Opposite enantiomers of limonene as major
constituents in the defensive secretion of related carabids. Naturwissenschaften 2009, 96, 1443–1449. [CrossRef] [PubMed]
Claridge, M.F. Stridulation and defensive behaviour in the ground beetle, Cychrus caraboides (L.). J. Entomol. Ser. A Gen. Entomol.
1974, 49, 7–15. [CrossRef]
Wheeler, J.W.; Chung, R.H.; Oh, S.K.; Benfield, E.F.; Neff, S.E. Defensive Secretions of Cychrine Beetles (Coleoptera: Carabidae).
Ann. Entomol. Soc. Am. 1970, 63, 469–471. [CrossRef]
Schildknecht, H. Die Wehrchemie von Land- und Wasserkäfern. Angew. Chem. 1970, 82, 17–25. [CrossRef]
Pearson, D.L.; Blum, M.S.; Jones, T.H.; Fales, H.M.; Gonda, E.; Witte, B.R. Historical perspective and the interpretation of
ecological patterns: Defensive compounds of tiger beetles (Coleoptera: Cicindelidae). Am. Nat. 1988, 132, 404–416. [CrossRef]
Kelley, K.C.; Schilling, A.B. Quantitative Variation in chemical defense within and among subgenera of Cicindela. J. Chem. Ecol.
1998, 24, 451–472. [CrossRef]
Blum, M.S.; Jones, T.H.; House, G.J.; Tschinkel, W.R. Defensive secretions of tiger beetles: Cyanogenetic basis. Comp. Biochem.
Physiol. Part B Comp. Biochem. 1981, 69, 903–904. [CrossRef]
Pearson, D.L. The function of multiple anti-predator mechanisms in adult tiger beetles (Coleoptera: Cicindelidae). Ecol. Entomol.
1985, 10, 65–72. [CrossRef]
Pearson, D.L. The Evolution of multi anti-predator characteristics as illustrated by tiger beetles (Coleoptera: Cicindelidae). Fla.
Entomol. 1990, 73, 67–70. [CrossRef]
Eisner, T.; Meinwald, Y.C.; Alsop, D.W.; Carrel, J.E. Defense Mechanisms of Arthropods. XXI. Formic Acid and n-Nonyl Acetate
in the Defensive Spray of Two Species of Helluomorphoides. Ann. Entomol. Soc. Am. 1968, 61, 610–613. [CrossRef]
Attygalle, A.B.; Meinwald, J.; Eisner, T. Defensive secretion of a carabid beetle, Helluomorphoides clairvillei. J. Chem. Ecol. 1992,
18, 489–498. [CrossRef]
Nenadić, M.; Soković, M.; Calhelha, R.C.; Ferreira, I.C.F.R.; Ćirić, A.; Vesović, N.; Ćurčić, S. Inhibition of tumour and non-tumour
cell proliferation by pygidial gland secretions of four ground beetle species (Coleoptera: Carabidae). Biologia 2018, 73, 787–792.
[CrossRef]
Dimkić, I.; Stanković, S.; Kabić, J.; Stupar, M.; Nenadić, M.; Ljaljević-Grbić, M.; Žikić, V.; Vujisić, L.; Tešević, V.; Vesović, N.; et al.
Bat guano-dwelling microbes and antimicrobial properties of the pygidial gland secretion of a troglophilic ground beetle against
them. Appl. Microbiol. Biotechnol. 2020, 104, 4109–4126. [CrossRef] [PubMed]
Giglio, A.; Brandmayr, P.; Dalpozzo, R.; Sindona, G.; Tagarelli, A.; Talarico, F.; Brandmayr, T.Z.; Ferrero, E.A. The Defensive
Secretion of Carabus lefebvrei Dejean 1826 Pupa (Coleoptera, Carabidae): Gland ultrastructure and chemical identification. Microsc.
Res. Tech. 2009, 72, 351–361. [CrossRef] [PubMed]
Attygalle, A.B.; Meinwald, J.; Liebherr, J.K.; Eisner, T. Sexual dimorphism in the defensive secretion of a carabid beetle. Experientia
1991, 47, 296–299. [CrossRef]
Holliday, A.E.; Mattingly, T.M.; Toro, A.A.; Donald, L.J.; Holliday, N.J. Age- and sex-related variation in defensive secretions of
adult Chlaenius cordicollis and evidence for their role in sexual communication. Chemoecology 2016, 26, 107–119. [CrossRef]
Holliday, A.E.; Holliday, N.J.; Mattingly, T.M.; Naccarato, K.M. Defensive Secretions of the carabid beetle Chlaenius cordicollis:
Chemical components and their geographic patterns of variation. J. Chem. Ecol. 2012, 38, 278–286. [CrossRef] [PubMed]
Schildknecht, H.; Koob, K. Zur explosionschemie der Bombardierkäfer. Naturwissenschaften 1969, 56, 328. [CrossRef]
Hefetz, A.; Lloyd, H.A.; Valdenberg, A. The defensive secretion of the tiger beetle Cicindela flexuosa (F.)(Cicindelinae; Carabidae).
Experientia 1984, 40, 539–540. [CrossRef]
Jacobson, M. Chemical insect attractants and repellents. Annu. Rev. Entomol. 1966, 11, 403–422. [CrossRef]
Life 2021, 11, 562
95.
96.
97.
98.
99.
100.
101.
102.
103.
104.
22 of 22
Schildknecht, H.; Holoubek, K.; Weis, K.H.; Krämer, H. Defensive substances of the arthropods, their isolation and identification.
Angew. Chem. Int. Ed. Engl. 1964, 3, 73–82. [CrossRef]
Xu, S.; Errabeli, R.; Will, K.; Arias, E.; Attygalle, A.B. 3-Methyl-1-(methylthio)-2-butene: A component in the foul-smelling
defensive secretion of two Ceroglossus species (Coleoptera: Carabidae). Chemoecology 2019, 29, 171–178. [CrossRef]
Moore, B.P.; Brown, W. V Chemical composition of the defensive secretion in Dyschirius bonelli (Coleoptera: Carabidae: Scarittnae)
and its taxonomic significance. Aust. J. Entomol. 1979, 18, 123–125. [CrossRef]
Schildknecht, H.; Winkler, H.; Maschwitz, U. Vergleichend chemische Untersuchungen der Inhaltsstoffe der Pygidialwehrblasen
von Carabiden. Z. Für Nat. B 1968, 23, 637–644. [CrossRef]
Schildknecht, H.; Maschwitz, U.; Winkler, H. Zur Evolution der Carabiden-Wehrdrüsensekrete. Naturwissenschaften 1968,
55, 112–117. [CrossRef]
Vesović, N.; Ćurčić, S.; Vujisić, L.; Nenadić, M.; Krstić, G.; Perić-Mataruga, V.; Milosavljević, S.; Antić, D.; Mandić, B.; Petković, M.
Molecular diversity of compounds from pygidial gland secretions of cave-dwelling ground beetles: The first evidence. J. Chem.
Ecol. 2015, 41, 533–539. [CrossRef] [PubMed]
Kanehisa, K.; Kawazu, K. Differences in neutral components of the defensive secretion in formic acid-secreting carabid beetles.
Appl. Entomol. Zool. 1985, 20, 299–304. [CrossRef]
Will, K.W.; Gill, A.S.; Lee, H.; Attygalle, A.B. Quantification and evidence for mechanically metered release of pygidial secretions
in formic acid-producing carabid beetles. J. Insect Sci. 2010, 10, 12. [CrossRef] [PubMed]
Scott, P.D.; Hepburn, H.R.; Crewe, R.M. Pygidial defensive secretions of some carabid beetles. Insect Biochem. 1975, 5, 805–811.
[CrossRef]
Schildknecht, H.; Holoubek, K. Die Bombardierkäfer und ihre Explosionschemie V. Mitteilung über Insekten-Abwehrstoffe.
Angew. Chem. 1961, 73, 1–7. [CrossRef]