The evolution of defence mechanisms in carabid beetles: a review

S. Casellato, P. Burighel & A. Minelli, eds. Life and Time: The Evolution of Life and its History. Cleup, Padova 2009.

The evolution of defence mechanisms in carabid beetles:

a review Pietro Brandmayr, Teresa Bonacci, Anita Giglio, Federica F. Talarico,

Tullia Zetto Brandmayr

Dipartimento di Ecologia, Università della Calabria, Ponte Bucci, I 87036 Arcavacata di Rende (Cosenza), Italy

Email: [email protected] Introduction Animals are continuously confronted with predation risk. This explains the defence mechanisms of various nature that have evolved. The evolution of antipredator behaviours has been extensively studied by many Authors in a large range of taxa. Alcock (1979) focused on three important factors in the evolution of antipredator behaviour: i) the species of enemies a possible prey has to face, ii) the level of danger each represents and iii) the costs to prey of possible defences.

On the other side, predators may become more and more effective so that a racing to armament may start using predator-specific counter-adaptations.

In carabid beetles, abiotic factors and predation represent the main causes of mortality in all life-cycle stages; additionally, pathogens and parasites can be important to some developmental stages (Lövei & Sunderland 1996).

In his survey of the most common species preying on carabids, Thiele (1977) reported insectivores as the hedgehog (Erinaceus europaeus) and the shrew (Sorex araneus); minor impact, the mole (Talpa europaea), probably because of its subterranean existence which favours at the most encounters with larval carabids. Bats (Myotis myotis) have been demonstrated to feed also from the ground so including carabids in their diet (Kolb 1958). Rodents as mice can exert a considerable influence on carabid populations. Among birds a large number of families prey at least occasionally on coleopterans including carabids, mostly birds of prey and owls probably because of the nocturnal habits of the most of them. Frogs (Rana arvalis; Zimka 1966), toads (Bufo americanus; Larochelle 1974) and lizards (Podarcis sicula; Bonacci et al. 2008a) exert important predatory pressure on carabids. Invertebrates as robber flies (Asilidae) have an important predatory role on Cicindelinae (Lavigne 1972), ants can regulate carabid populations not only by predation but also by strong habitat competition, while only some of the spiders include carabids in their diet, but literature data are not very rich. Some large coleopterans can also prey on carabids: in the lab we observed the predatory

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behaviour on many carabid species by the rove beetle Ocypus olens (Staphylinidae) (Bonacci et al. 2006).

Against such a large spectrum of possible enemies carabids present different defence strategies in all their biological stages, from the larval to the pupal and the adult. The most important among these strategies are reviewed here, under three separate headings, i.e. chemical, morphological and behavioural mechanisms. Chemical defence strategies In this section we consider as chemical defence strategies both the release of chemical substances to as an active reaction against a possibly predator and the chemical mimicry which conversely prevents predator aggressive behaviour.

Glandular defences

Carabids possess pygidial glands which produce defensive secretions. These glands exhibit are very diverse in structure and even in the nature of the produced substances (Thiele 1977). The mode of discharge is either by oozing, spraying or crepitation. Oozing is probably the plesiotypic mode of discharge, with active spraying and crepitation as later refinements (Moore 1979).

The major function is probably the defence against predators (see Evans & Schmidt 1990 and references therein), but also facilitation of the penetration of the defensive compounds into the predator’s integuments, antimicrobial and antifungal activity, alarm messages can also be obtained this way.

A comparative study of the secretions of carabid pygidial glands was made by Schildknecht et al. (1968). Moore (1979) listed all the principal groups detected in carabid tribes: hydrocarbons, aliphatic ketones, saturated esters, formic acid, higher saturated acids, unsaturated acids, phenols (m-cresol), aromatic aldehydes (salicylaldehyde) and quinones (see also Evans & Schmidt 1990). According to the class of substances they produce, carabids can be roughly divided into six groups: 1) isovaleric acid and isobutyric acid (Broscini, Scaritini, several Bembidiini), 2) methacrylic acid and tiglinic acid (Carabinae, Cychrini, Pterostichini, Amarini), 3) formic acid (Agonini, Harpalini, Licinini, Lebiini, Dryptini, Zuphiini), 4) quinones (Clivina, Chlaeniellus) 5) m-cresol (Panagaeini, Chlaeniini) and 6) hydroperoxide and hydroquinone (Brachininae) (Wheeler et al. 1970; Thiele 1977; Kanehisa & Murase 1977).

Carabid beetles such as bombardier beetles of the genus Brachinus, are able to release irritating quinones, produced by oxidation of hydroquinones in a double-chambered apparatus (Schildknecht 1961; Schildknecht et al. 1968; Aneshansely et al. 1969; Eisner & Aneshansely 1999; Eisner et al. 2000); a certain amount of heat and the explosion associated with the reaction reinforce the defensive effect.

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Predation on these beetles appears to be rare (Juliano 1985). From the literature it is known that Anchomenus dorsalis produces toxic methylsalycilate from its pygidial gland (Schildknecht 1970). Tiger beetle species living in habitats with large water availability produce benzaldehyde (Altaba 1991).

The carabid beetle Galerita lecontei secretes as a spray a mixture of formic acid, acetic acid and lipophilic components (long-chain hydrocarbons and esters) (Rossini et al., 1997). Biosynthesis of tiglic and ethacrylic acids from isoleucine via 2-methylbutyric acid was demonstrated in Pterostichus californicus (Attygalle et al. 2007).

The taxonomic distribution among beetles of the chemical classes shows that formic acid or relative strong irritants are found in tribes with a high species diversity in tropical regions, whereas those with high species diversity in temperate regions use milder saturated/unsaturated carboxylic acids (Will et al. 2000). Although exocrine glands and their defensive secretions are well investigated in adults, up to recent date no information was available about larvae and pupae which are the most vulnerable stages of the life cycle.

In a recent paper, we described for the first time the chemical defensive strategy in the pupa of Carabus lefebvrei, which relies on substances secreted by abdominal glands (Fig. 1) (Giglio et al. 2009). The chemical analyses of the gland secrete revealed a mixture of low molecular weight terpenes as well as ketones, aldehydes, alcohols, esters and carboxylic acids, which in adults have been regarded as deterrent against predators. Monoterpenes, specially linalool, were the major products in pupal stage of C. lefebvrei (Table1). We suggested that this gland secretion has both a deterrent function against the predators and a prophylaxis function against pathogens. The pupal stages of carabid beetles are known so far to have no physical protections, thus the chemical protection provided by the abdominal glands is very important for species survival. Their habitat is very rich in bacterial and fungal microorganisms, some species of which are possible pathogens for insects. Besides, the highly lipophilic nature of monoterpene compounds suggests that their principal targets are bacteria and/or fungi cell membranes.

Non-glandular defences

Comparable to the use of non-glandular defences reported for arthropods (blood factors, enteric discharge, detachable structures; see Eisner 1970), many carabids when handled or otherwise disturbed regurgitate (Forsythe 1982) or defecate.

Chemical mimicry With this strategy, carabids living in or near the nest of social insects change their cuticular profile, thus avoiding be detected by the nest residents. Chemical

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mimicry is widespread. Living in the nest of social insects is indeed profitable for several reasons (food, protection, etc.). Here we treat only cases of chemical mimicry toward the ants, the only social insects known to be parasitized or preyed upon by carabids. By means of trophallaxis and grooming, members of an ant colony maintain the colony odour which is used to distinguish nestmates from non-nestmates (Lenoir et al. 2001). The only cases described up to date in carabid beetles involve the larvae of Thermophilum sp. (Dinter et al. 2002) and the adults of Siagona europaea (Zetto Brandmayr et al. 2005; Talarico et al. in press). Thermophilum larvae spend their life in ant nests preying on ants or their brood; prey hydrocarbons appear in the carabid cuticula after it has fed on ants, this allows the beetle to freely move within the host colony (Dinter et al. 2002).

Fig. 1 (A) Lateral view of C. lefebvrei pupa; I-IX abdominal segments; Black square show one spiracle with a glandular area. (B) Scanning micrograph is a detail of A showing pore openings of the glands (white head arrow) close to the spiracle (sp). (C) Detail of the pore openings with secretion (head arrow). Bars: 10 mm (A), 500 µm (B), 10 µm (C). (from Giglio et al. 2009).

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Tab. 1 Peaks identification of gland secretion of Carabus lefebvrei pupae (N=5) (data from Giglio et al. 2009).

Peak Retention time (min)

% N=5 Identification

1 4,95 0,18 pivalic acid 2 8,175 0,08 p-benzoquinone 3 8,318 0,48 alfa-pinene 4 8,819 0,20 camphene 5 9,291 0,13 benzaldehyde 6 9,882 0,79 6-methyl-5-hepten-2-one 7 9,976 2,97 beta-pinene 8 10,29 0,69 2-carene 9 10,517 0,60 alfa-phellandrene 10 10,84 5,42 alfa-terpinene 11 11,093 0,88 orto-cimene 12 11,222 0,96 limonene 13 11,398 0,46 cis-ocimene 14 11,722 0,50 trans-ocimene 15 11,793 0,79 2-hydroxy benzaldehyde 16 13,365 77,98 linalool 17 13,655 0,10 3-nonen-1-ol (nonanal) 18 14,853 0,10 camphor 19 15,728 1,24 4,8-dimethyl-3,7-nonadien-2-ol 20 16,128 0,14 1-(1-oxobutyl)-1,2-dihydropyridine 21 16,249 1,06 3,4-di(1-butenyl)-tetrahydrofuran-2-ol 22 17,437 0,36 thymol methyl ether 23 17,824 0,03 phenylacetic acid

24 20,424 0,72propanoic acid, 2-methyl-,2,2-dimethyl-1-(2-hydroxy-1-methylethyl)propyl ester

25 21,04 1,01 propanoic acid, 2-methyl-, 3-hydroxy-2,4,4-trimethylpentyl ester

26 21,514 0,90 beta-elemene 27 22,266 0,40 alfa-santalene 28 22,603 0,23 trans-alfa-bergamotene

29 26,287 0,50 pentanoic acid, 2,2,4-trimethyl-3-carboxyisopropyl,isobutyl ester

30 27,157 0,05 dodecanoic acid, 1-methylethyl ester 31 29,508 0,06 sclarene

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Conversely, S. europaea does not live inside ant nests but in soil crevices from where it preys on incoming ants at ambush (for more detail, see Bauer et al. 2005; Zetto Brandmayr et al. 2007).

Gas chromatography analyses revealed that extra compounds are present on the carabid cuticle after predation, these compounds being those of the tested ants (Fig. 2). We suggest that this may be an intermediate evolutionary stage towards a true myrmecophilous life style as evolved in some tropical carabids (Talarico et al. in press).

Fig. 2 Gas-chromatographic plot of: A) unfed and isolated Siagona europaea; B) Tapinoma nigerrimum ants; C) Siagona europaea after ant consumption. (data from Talarico et al. in press).

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In other carabids with myrmecophylous or myrmecophagous habits as the Paussini, a true chemical mimicry is not demonstrated to date, although appeasing substances are secreted by beetles to avoid triggering the ants’ aggressive behaviour (Geiselhardt et al. 2007). Morphological strategies Cryptism, aposematism and mimicry

Animals have evolved a variety of morphological strategies to avoid or reduce predation; basically, these develop along two different pathways: those making the animals hard to find (cryptic behaviour) and those enhancing escaping possibility, when detected by predators (Alcock 1979). A peculiar adaptation deriving from the first kind may be considered the true opposite behaviour, that is to become very conspicuous to predators. A possible outcome is aposematism, very common among insects.

As for the first solution (cryptic behaviour) carabids are less likely than other insects to evolve similarity to leaves or twigs, but thanks to their dark brown colours many of them can blend into the general background and are therefore overlooked by the predators. Some Cicindelinae species are hardly distinguishable from the sandy soils on which they live, most of all when they remain motionless.

Many animals use warning colours to signal their dangerousness to potential predators (Cott 1940; Guilford 1990). Aposematic colours decrease the likely of attack from naïve predators, either as effect of the novelty and of aversive colours (Coppinger 1969, 1970; Roper and Cook 1989; Gamberale and Tullberg 1996 a, b) or both (Sillén-Tullberg 1985).

Many cases of carabid aposematism have been reported by Lindroth (1971) for the Lebiini, e.g. in the genus Lebia, where L. viridis is suspected to prey on tree-dwelling Alticinae (flea beetles). Lindroth supposes also that some South African Lebistina species exhibit Batesian mimicry in respect to the flea beetles Diamphidia and Polyclada, which are so poisonous as to be used by hunting Bushmen in the preparation of an arrow poison to kill warm-blooded animals. A similar black-and-yellow pattern is found in Eurycoleus larvae, which prey on the pupae of an endomychid beetle (Erwin and Erwin 1976).

Mimicry in Cicindelini and Graphipterini has been reported from arid biotas of Eastern and Northern Africa, in which some tiger beetle species (Elliptica flavovestita, Lophyra wajirensis, Neolaphyra leucosticta) are found to have colour patterns identical to the sympatric Graphipterus populations. It is thought that Cicindelids could be here the less protected (Batesian) partecipants in a “classic” (Müllerian) mimicry association, where Graphipterus may be unpalatable to Vertebrate predators (Cassola & Vigna Taglianti 1988).

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Unlike most carabid beetles which are homogeneously brown or brown-black, a number of Brachinus species are bright orange-red with blue or green elytra; this is likely an aposematic signal (Bonacci et al. 2008a). Also Anchomenus dorsalis, which we often find aggregated with Brachinus sp. (see the next paragraph) exhibits a bright two-coloured coat (green-blue and red-brown). We tested in Lab the effectiveness of this aposematism with different predators as the rove beetle Ocypus olens (Bonacci et al. 2006), the shrew Crocidura leucodon (Bonacci et al. 2004a), and the lizard, Podarcis sicula (Bonacci et al. 2008a) to which bright coloured or cryptic brown carabid beetles were offered as preys. All the experiments revealed a significant predator preference of the predator for non visually conspicuous prey. Since both Brachinus sp. and Anchomenus dorsalis are chemically protected, this may be interpreted as a Müllerian mimicry.

Moreover, we investigated the cuticular composition of A. dorsalis, B. sclopeta and Poecilus cupreus (Bonacci et al. 2008b). Poecilus cupreus, a non-aposematic carabid commonly found in aggregations of Brachinus spp. and Anchonemus dorsalis, was used as a control. The cuticular profiles of the three species include 48 different hydrocarbons. The cuticular hydrocarbon profiles of the three species of carabids were different, with Brachinus being however chemically more similar to Anchomenus than Poecilus; in turn, the hydrocarbon profile of Poecilus was more similar to that of Anchomenus than to the one of Brachinus. We suggest that A. dorsalis is possibly mimicking also the cuticular profile of B. sclopeta as a more effective antipredator strategy, both versus visual and tactile/olfactory predators. Behavioural strategies Gregariousness Living in groups can also be adaptive in avoiding predation by visually hunting predators and many possible antipredator advantages can be shared by animals which clump together. The individual risk to be killed is lowered, depending on group size, when the predator is satiated (Alcock 1979). In some Indian species of Cicindelinae (tiger beetles), as Calomera plumigera and C. chloris, a sort of “com-munal roosting” has been described (Uniyal & Bhargav 2007). These diurnal roosts were found on two shrub plants (Syzygium and Carissa) in a riverine area of the Simbalbara Wildlife Sanctuary of Himachal Pradesh, limited to the first monsoon months (June and July), and are formed by many thousand adults. Roosting tiger beetles seemingly expose the abdomen outwards, thus increasing the effect of chemical defenses (benzaldehyde and benzoyl cyanide) against predators. In insects, aposematism often occurs together with gregariousness (Edmunds 1974). Some authors suggested that the gregariousness increases the effect of the

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aposematic signal (Poulton 1890; Cott 1940) and this increasing in signal efficiency could influence both the initial unconditioned aversion of naïve predators and the speed and memorability of avoidance learning (Gamberale & Tullberg 1998).

Among carabid beetles, adaptive relationships are known, for example gregariousness, i.e. some individuals associate with others of the same species as well as of different ones at least during some periods of their life cycle (Thiele 1977).

Aggregation has been described for adults of Anchomenus dorsalis (Allen 1957), Nebria brevicollis and Brachinus crepitans (Greenslade, 1963), Brachinus sclopeta and Brachinus explodens (Wautier 1971), Brachinus variventris (Zaballos 1985) and Colliuris batesi, a carabid beetle inhabiting central Amazonian forests (Adis et al. 1997).

Metrius contractus is a non-aposematic bombardier beetle which discharges its defensive secretion as a froth that clings to its body. Aggregation in laboratory has been described by Eisner et al. (2000).

On the whole, aggregation seems to occur in only a few carabid species and its evolutionary significance may be mainly protection from water loss and keeping together of the sexes (Thiele 1977) as well as the lowering of individual predation risk (Alcock 1979).

A. dorsalis is usually found in small groups inside the aggregations of Brachinus and Chlaenius species (Lindroth 1949; Juliano 1985; Zaballos 1985; Bonacci et al. 2004b; Mazzei et al. 2005). Lindroth (1949) observed also interspecific interactions among members, recently described in detail as “rubbing behaviour” by Zetto Brandmayr et al. (2006) (Fig. 3).

In the last years we studied carabid aggregations in Calabria (South Italy). The dominant species are aposematic and chemically protected: Chlaenius chrysocephalus (60% of total carabid specimens in the aggregation), Brachinus brevicollis (14,84%), B. crepitans (8,63%), Anchomenus dorsalis (5,52%), B. psophia (4,66%), B. sclopeta (2,015%) (Bonacci et al. 2004b; Zetto Brandmayr et al. 2008).

To the general advantages provided by gregariousness, further increase in effectiveness against predators can be postulated for aposematic insects: (1) in interspecific aggregations more success depends on the Müllerian mimicry, when two or more protected species share a similar warning pattern; in this form of mimicry the mimics possessing different defence chemicals are better protected than those that share a single defence chemical (Skelhorn & Rowe 2005) and (2) the possibility of repelling predators (also in intraspecific aggregations) is more prolonged in the time. Indeed, bombardier beetles may discharge their defensive spray a number of times, after which they are temporally unprotected, as we observed in our experiments with lizards and shrews (Bonacci et al. 2004a, 2008).

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Feeding behaviour All animals have to face the trade-off between efficiency of foraging and minimizing its costs in terms of energy consumption and the risk to be preyed while eating.

One protective strategy to reduce risk is to ambush for prey, i.e. to remain concealed in a burrow from which approaching prey is sized. A few cases of ambushing are described for carabids typically for Cicindelinae larvae and for larval Sphallomorpha (Moore 1974; Erwin 1981) which possess dorsal abdominal anchorage pegs that allow them to attack vertically in the burrows. Adult Siagona europaea ambush for ants from clay crevices where the captured prey is dragged into and repeatedly waved around on the beetle’s body before consumption. This probably gains to the beetle the protective odour similar to that of the ants (Zetto Brandmayr et al. 2005; Talarico et al. in press).

Fig. 3 Rubbing behaviour in Brachinus sclopeta and Anchomenus dorsalis (above in the picture) (data from Zetto Brandmayr et al., 2006).

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In the larva of the largest ground beetle of Europe Carabus (Procerus) gigas a preying behaviour called “trapdoor camouflage” has been described (Brandmayr & Zetto Brandmayr 1983) (Fig. 4). After seizing the prey (a snail), when the latter went lame, the larva digs out an U-shaped burrow in the soil and re-emerges near the shell. Thereafter the snail is re-located by the larval mandibles and the shell’s mouth closes the tunnel like the lid of a trapdoor (Zetto Brandmayr & Brandmayr 1998).

Predation on ant broods in their nests has been evolved in the larva of Graphipterus serrator which remains concealed in burrows dug directly below the brood. The liquid food, as egg content or larval haemolymph, is sucked up through a mandibular suctorial channel by simply protruding the head from the burrow in the first instar, while aged instars are supposed to be able to transport the brood inside the burrow. (Zetto Brandmayr et al. 1994 a, b).

Fig. 4 Feeding behaviour of Procerus gigas larva (scale: 1 cm) (reproduced from Zetto Brandmayr and Brandmayr 1998).

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Re-location of the food has been observed also in larval seed-eating carabid

beetles: Ophonus spp. (Brandmayr Zetto & Brandmayr 1975; Zetto Brandmayr 1976) and other Harpalinae (Alcock 1976). In this case the larva, which has previously dug a burrow, introduces into it a number of Daucus carota seeds which, before being eaten, need some manipulation as the removal of the external seed layers. The adaptive value of this behaviour is outstanding since it significantly reduces the time the larva spends on the soil surface, where it has no protection against enemies.

Finally, we consider a particular mechanisms probably evolved to avoid larval cannibalism. If reared together, all carabid larvae tend to attack other larvae, conspecifics included. This fact is well known to carabidologists (Paarmann 1966; Zetto Brandmayr 1976; Thiele 1977; Brunsting & Hessen 1983; Nelemans 1987; Currie & Digweed 1996; Currie & Spence 1996; see also Lövei & Sunderland 1996 for a review).

Recently we investigated aggressive and cannibalistic behaviour in the larvae of eight ground beetle species, especially Chlaenius velutinus and C. spoliatus, whose larvae have long articulated cerci. (Zetto Brandmayr et al. 2004; Bonacci et al. 2005). Chlaenius species live in dense populations with frequent intra-specific encounters, something rare in other carabid species.

Pairs of conspecific larvae of the eight ground beetles species were tested for aggressive and cannibalistic behaviour. Unlike the other six species, larvae of the two Chlaenius species avoid cannibalism, possibly as a consequence of a behavioural display involving cerci interactions. This display was never recorded in conspecific larval interactions of the other species. The cerci interaction probably inhibits cannibalism via intra-specific recognition; this behaviour may have evolved under the pressure of ecological factors (resource abundance and dispersion, larvae density, frequency of encounters).

Stridulation The sound production by carabids has been less extensively investigated than other behavioral components of defense. Stridulation or chirping is known for Cicindela (Freitag & Lee 1972), Elaphrus (Bauer 1973), Cychrus (Claridge 1974; Thiele 1977; Greven & Heuwinkel 2005), Scaphinotus (Greene, 1975), Carabus (Bauer 1975). Sound production is anyway reported for a wide variety of genera and can be generated by different apparatuses. The most accepted adaptive interpretation of stridulation is additional defence against larger predators, found by Bauer (1976) by observing common sand pipers (Actitis hypoleucos) capturing Elaphrus cupreus individuals after their stridulation apparatus was removed.

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Conclusions To conclude, carabid beetles have evolved antipredator defence mechanisms which rely on biochemical, morphological and behavioural components. Higher survival rate is however assured to tree-dwelling carabids by basically morphological traits such as narrow body shape, dorso-ventral flattening, large eyes and long legs (Stork 1987). Moreover, inactive beetles rest at safe sites, under stones, in crevices, in the soil or on undersides of leaves; night activity is also thought to be an antipredator defence (Lövei & Sunderland 1996).

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