The effects of carabid (Coleoptera: Carabidae) on the fauna of wheat fields in Chile

R. Carrillo1, R. Alarcón2 & M. Neira1 1 Instituto de Producción y Sanidad Vegetal, Universidad Austral de Chile, Casilla 567, Valdivia, Chile; rcarrill@uach. cl. Fax 56-63-221233 2 Universidad de San Carlos, Mazatenango, Suchitepequez, Guatemala.

Received 21-Xi-2020. Corrected 23-iX-2005. Accepted 28-viii-2006.

Abstract: The role of carabid beetles in reducing populations of phytophagous has been an elusive subject. A field experiment was established on a commercial wheat crop (cv. Otto) with an area of 4.5 ha in Valdivia, Chile, during the spring and summer of 1996-1997. The field had been under a prairie system for two years, before wheat sowing (fertilization and a pesticide had been applied during crop development). Samples were taken at approxi- mately monthly intervals. Carabid beetles were sampled with a grid of pitfall traps and other insects were sampled with a vacuum net and soil cores. The genera of the carabids found are of neotropical origin. Exclusion by polythene barriers, together with removal of carabid beetles using traps, was an effective technique for controlling carabid populations in a commercial wheat crop. A reduction in the number of carabid beetles was associated with an increase in the number of springtails and arachnids, and a decrease of agromyzid adults. Phytophagous insects, such as homopterans and lepidopterous larvae, were not affected by carabid exclusion and removal. The action of carabid beetles on the arthropod fauna can be extremely complex, due to its predatory activity at multitrophic levels. Rev. Biol. Trop. 55 (1): 101-111. Epub 2007 March. 31.

Key words: Carabids, phytophagous insects, multitrophic interactions, conservative biological control, preda- tor-prey interaction.

The role of carabid beetles in reducing studies of Wright et al. (1960) and Coaker populations of phytophagous insects has (1965), showed that the survival of immature been a very elusive subject. According to stages of the cabbage root fly was negatively Lövei and Sunderland (1996), the effective- related to the number of predatory carabids ness of a natural enemy can be established present on Brassica plots. Edwards et al. following four sequential steps: (1) evaluat- (1979), found a negative relationship between ing dynamics and correlating predator and numbers of polyphagous predators and aphids prey density, (2) obtaining evidence of a in cereals in England. Other studies, however, trophic link between the prey and the preda- have failed to find a relationship between the tor, (3) manipulating predator numbers and presence of carabids and the populations of the effect on prey density, and (4) integrat- phytophagous insects. ing the above information to quantify the The main aim of the present study is to effect of predator on prey. evaluate the effect of carabid beetles (the gen- Most studies on carabids and their prey era of the carabid fauna found has a neotropi- are of the first or second type, fewer inves- cal origin) on the wheat arthropod fauna by tigators have considered steps 3 and 4. The manipulating abundance.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (1): 101-111, March 2007 101 MATERIALS AND METHODS two days, in each trapping period. The ento- mofauna was vacuum sampled with a vacuum A field experiment was established on a insect net and soil cores. Twenty five 0.092 m2 commercial wheat crop (cv. Otto) with an area D-Vac samples and the same number of soil of 4.5 ha, at the Universidad Austral de Chile, cores 0.20x0.20x0.15 cm were taken within Experimental Station, Valdivia, Chile (39º45’ each plot. Samples were taken to the laboratory S, 73º14’ W) during the spring and summer of in plastic bags. There they were passed through 1996-1997. The field had been under a praire a sieve and then the entomofauna was extracted system for two years, before wheat sowing. by hand sorting. Fertilization included chilean nitrate, superphos- phate and potassium chloride, at 149-184-96 kg NPK ha-1. The field was treated with glyphosate RESULTS 1.2 kg i.a. ha-1, previous to being ploughed and sown to winter wheat in July 1996. The only The number of carabids caught in each pesticide applied during the crop development treatment (Table 1) (Fig. 1 y 2) shows that was MCPA at 0.75 l i.a. ha-1. significantly (p<0.05) fewer individuals were Twelve plots measuring 2x3 m, arranged in a ran- 250 domized block design of four replicates of three treatments 200 each, were sampled regu- larly with a vacuum insect 150 net (D-Vac), pitfall and soil cores from September 1996 100 to January 1997. number of carabids The treatments consisted 50 of carabid isolation, carabid isolation and exclusion, and 0 an unisolated area referred to as the control. Carabid isola- tion was obtained by digging Fig. 1. Total number of carabid beetles caught in each pitfall traps in each of the a trench around the plots and treatments; Exclusion y-y exclusion and removal ∆-∆ and control Ο-Ο. erecting a 35 cm high poly- thene barrier supported by 12 wooden sticks and buried to a depth of 10 cm. Exclusion 10 was obtained through three pitfall traps per plot, which 8 were kept open throughout 6 the experimental period. Samples were taken at 4 approximately monthly inter- number of carabids vals. Carabid beetles were 2 sampled with a grid of three pitfall traps, e.g. plastic jars 0 9.5 cm in diameter, with formaldehyde as preservative. Fig. 2. Number of carabid beetles extracted from soil cores in each of the treat- Traps were left in the field for ments; Exclusion y-y exclusion and removal ∆-∆ and control Ο-Ο.

102 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (1): 101-111, March 2007 2 1 0 3 0 0 0 0 0 0 0 0 0 6 R 3 1 3 0 0 0 0 0 0 0 0 E 11 10 28 30-01 9 9 0 0 0 3 0 0 0 0 C 11* 53** 119** 204** 1 0 0 0 0 0 0 0 0 0 0 1 0 2 R 2 4 1 1 0 1 0 0 0 0 0 0 2 E 11 26-12 7 2 0 0 0 2 C 6* 8** 13** 29** 24** 40** 20** 151** 0 0 0 0 0 0 0 0 0 1 0 0 1 2 R 1 0 0 0 1 0 1 1 3 0 0 0 3 9 E 2-12 4 0 0 0 0 2 1 0 C 11 6** 19** 13** 19** 76** 0 0 0 0 0 0 0 0 0 0 0 1 0 1 R Sampling dates 0 0 0 1 0 0 0 1 1 0 0 1 0 4 E 15-11 0 0 1 0 0 0 7 0 0 0 1 C 10* 3** 22* TABLE 1 TABLE 0 0 0 0 0 0 0 0 0 0 0 0 0 0 R 0 0 0 0 0 0 0 1 0 0 0 0 0 1 E 31-10 2 0 4 0 0 0 2 0 0 0 0 C 4** 4** 16** 0 0 2 0 0 0 0 0 0 0 0 0 0 2 R 4 0 2 2 0 0 0 0 0 0 0 0 1 9 E 16-10 3 0 1 0 0 0 2 0 0 0 1 C 6* 4** 17* (Sol.) Montreh (Dej.) Dej. (Dej.) (Dej.) (Dej.) (Sol.) Dej. (Dej.) Carabid Number and species of carabids caught in pitfall traps in (C), control untreated exclusion barrier (E) and exclusion barrier and (R), removal treatments sp. Dej. larvae (Dej.) larvae Argutoridius chilensis Argutoridius Calosoma vagans viridis Crossonychus aerea Feroniomorpha C. vagans aerea F. Metius flavipes cyaneus Mimodromites Parhypates Parhypates tenuistriatus Systolosoma brevis nigripennis Trechisibus unistriatus Trirammatus Total Significantly at * P≤0.05; ** P≤0.01

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (1): 101-111, March 2007 103 found in the exclusion, and exclusion and exclusion technique for manipulating the num- removal plots, in relation to the control plots. ber of carabids to establish their role in regulat- The results obtained confirmed that polythene ing prey numbers, has been employed by many exclusion barriers are an adequated method researches (Coaker 1965). This study supports for manipulating carabid density. Considerable previous experimental data, but also shows variation in the number of carabids trapped that this technique is appropiate for removing throughout the study period was observed. flying carabids such as C. vagans. Results sug- The variation could be related to climate (eg. gest that for this species, dispersal inside fields, a steady increase in temperature), during the after landing, occurs principally by ground sampling period. Calosoma vagans Dej., a movement. The large number of C. vagans large beetle, was the most numerous carabid found in control plots and their absence from trapped, in spite of being found only during the exclusion plots suggest that this large species last three sampling periods. is highly mobile on the ground. It seems likely Pitfall traps also caught, numerous other that many of the individuals caught inside con- arthropod groups (Table 2). The most abundant trol plots came from adjacent areas, rather than were staphylinid beetles, noctuid larvae and from a large population of this species in the arachnids. Soil cores did not show an effect of control plots. the treatments on the non carabid arthropod The effect of carabids on the arthropod fauna (Table 3). The effect of polythene barriers fauna: carabid exclusion did not affect the on the non carabid arthropod fauna in general number of homopterans, even though there was less marked than on the carabid fauna. are many reports from Europe that polypha- Only three groups showed statistically sig- gous predators (such as carabids), can restrain nificant differences in the number of individu- some homopterans, (such as cereal aphid pop- als collected by D-Vac; they were arachnids, ulations) at low level. The discrepancy of springtails and agromyzids. (Table 4) Springtails the results obtained in this study may be showed a marked increase in number, when the explained despite the aphid species being simi- carabid population was excluded and removed. lar in Chile and Europe [Sitobion avenae, S. Another group that had a similar pattern was fragarie (Walker) Metopolophium dirhodum the arachnid population. On the other hand the (Walker), M. festucae var cerealium (Stroyan) number of agromyzid flies was lower in the and Rhopalosiphum padi L.] (Carrillo and exclusion and removal treatment, than in control Zúñiga 1974, Stary 1993), by two main fac- plots. Groups of important phytophagous insects tors. In Chile, cereal aphids are controlled such as aphids, leafhoppers and noctuid larvae, efficiently by introducing aphidiine parasit- did not show significant differences in number oids (Norambuena 1981) which keep aphid among the test and control groups. populations at a very low density. In the current Because D-Vac sampling is unable to research aphidiine were found in large numbers estimate adequately the effect of treatments on (Table 4) and were not affected by exclusion the larger insects, such as last noctuid larvae barriers. An alternative explanation is that the instars, soil cores from the different treatments relationship of carabids with cereal aphids were hand sorted. Nonetheless, no effect was is a new one, because genera of the carabid found on the number of arachnid and noctuid fauna found has neotropical origin (Reichardt larvae in the different treatments (Table 3). 1977) and cereal aphids are of holartic origin (Szelegiewics 1965, Blackman and Eastop 1985). Introduction of most species of cereal DISCUSSION aphids to the neotropical area, occurred only from the mid 1960s onward (Zúñiga 1967, The efficacy of polythene barriers: Lara and Zúñiga 1969). However, given the the use of polythene barriers as an effective rather unselective feeding behaviour of ground

104 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (1): 101-111, March 2007 0 7 0 0 0 1 1 0 R 0 8 6 0 2 2 1 5 E 30-01 0 5 0 0 1 1 1 C 12 1 0 5 0 1 R 11 49 21 2 1 8 1 0 4 E 69 27 26-12 1 1 2 4 6 C 34 88 72* 1 0 4 0 0 4 0 R 44 1 3 9 0 0 0 E 11 39 2-12 0 2 7 0 0 4 0 C 51 0 0 0 0 0 0 0 0 R Sampling dates 0 0 0 0 0 1 0 0 E 15-11 TABLE 2 TABLE 0 0 0 0 0 0 0 0 C 0 0 0 3 0 0 1 0 R 1 0 0 7 0 0 2 0 E 31-10 1 0 0 0 0 0 3 0 C exclusion barrier (E) and exclusion barrier and (R), removal treatments 0 0 0 0 0 0 1 0 R 0.01 0 0 0 0 0 0 0 0 E < 16-10 Number of insects (excluding carabids) arachnids and chilopods caught in pitfall traps (C), control untreated 3 3 8 1 2 0 1 0 C 0.05; ** P <

1 Coleop t er a Coccinellidae Curculionidae Staphylinidae orders Aphididae Dermaptera larvae Noctuid Other Arachnids Chilopods Significantly different at * P 1 Mites are excluded. Ot her inse ct

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (1): 101-111, March 2007 105 2 1 7 0 3 0 R 12 20 35 3 0 0 4 5 2 E 27 21 20 30-01 0 1 5 9 6 3 1 C 29 22 3 1 8 8 0 5 R 10 31 22 2 3 1 0 2 E 11 11 30 20 26-12 3 2 0 9 1 0 C 20 22 21 2 0 0 0 0 6 0 R 10 10 7 0 3 3 0 2 E 27 16 13 2-12 8 0 0 8 0 0 C 18 20 19 1 0 2 0 1 1 R 11 14 21 Sampling dates 1 0 1 0 0 4 1 E TABLE 3 TABLE 14 35 15-11 0 0 0 0 0 1 4 0 C 13 0 5 0 0 0 0 0 0 R 15 0 0 0 0 0 0 0 0 E 12 31-10 exclusion barrier (E), exclusion barrier and (R), removal treatments 0 1 0 0 0 0 0 0 C 10 6 0 0 0 0 0 0 0 0 R 0 0 0 0 0 0 0 0 0 E 16-10 Number of insects (excluding carabids), arachnids and chilopods extracted soil from in (C), cores, control untreated 6 0 3 0 0 0 0 0 0 C

1 Carabid Ot her inse ct Curculionid larvae Curculionid pupae Curculionidae Scarabaeidae larvae Staphylinidae Coccinellidae orders Noctuid larvae Other arthropods Arachnids Chilopods 1 Mites, are excluded. Coleop t er a

106 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (1): 101-111, March 2007 5 0 0 0 0 1 0 2 3 0 0 0 R 49 150 330 3 0 0 0 0 2 0 5 1 0 2 0 E 74 21 298 30-01 4 3 0 0 0 1 0 5 0 0 0 C 11 65 55 351 1 0 2 1 0 1 1 0 0 R 16 39 20 21 17 263 8 1 0 1 1 0 4 9 0 0 E 70 27 38 16 173 26-12 ) 2 0 0 0 0 0 2 5 2 0 C 30 30 37 70 19 352 7 2 3 2 5 2 1 2 R 55 10 17 26 294 2257 1472 9 7 3 5 0 0 1 1 3 6 E 30 29 247 2-12 1052 1859 3 7 2 2 3 4 1 3 2 C 71 27 22 277 1050 1462 ) 2 3 3 2 3 1 3 1 R 25 21 45 17 43 409 658* Sampling dates Continued 0 3 8 1 8 0 2 0 0 6 E ( 36 16 42 644 335 15-11 3 0 8 1 2 4 2 5 C 72 32 18 10 69 840 715* TABLE 4 TABLE 0 0 1 0 1 1 0 0 2 7 R 10 97 46 604 530* 6 0 0 0 0 1 0 1 0 2 4 E 24 309 188 627 31-10 0 1 4 0 4 3 0 3 4 2 C 46 52 45 501 1245 7 0 0 2 0 1 0 0 0 7 1 1 R 71 68 340 exclusion barrier (E) and exclusion barrier and (R) removed (Number treatments per 9.2 m 8 0 0 1 0 1 0 0 1 0 0 E 11 87 310 147 16-10 7 0 0 0 0 0 0 0 0 9 2 2 C 66 Effect of manipulating carabid abundance number on number in (C), control of untreated collected arthropods by D-Vac 113 430 A A ER T Carabid OLEOP HO M OP T ER A LEPIDOP T ER A C DIP T ER A Aphididae Cicadellidae Noctuid larvae Other lepidoptera larvae Gelechiidae Coccinellidae larvae C OLLE MB OL A Lathridiidae Ptiliidae Staphylinidae Curculionidae Agromyzidae Lonchopteridae Anthomyiidae Sphaeroceridae

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (1): 101-111, March 2007 107 0 0 0 0 0 0 0 0 0 5 0 0 0 0 0 R 19 0 0 0 0 0 0 0 1 0 3 0 0 0 0 0 8 E 30-01 4 0 0 0 0 0 0 0 0 4 0 0 0 0 0 C 22 6 1 0 2 0 3 2 0 3 2 2 5 0 7 R 95 381 6 0 0 2 0 1 0 1 0 4 4 1 0 5 E 75 488 26-12 ) 2 0 0 6 1 0 0 1 1 0 0 5 C 11 10 10 109 509 0 2 0 2 2 0 3 7 0 9 4 R 68 12 23 12 226 1 1 2 3 0 0 6 0 1 6 2 0 E 46 25 10 229 2-12 0 2 5 3 2 6 5 4 4 1 3 1 C 54 12 21 279 ) 2 1 0 0 1 6 0 0 2 0 0 2 3 0 R 31 91 Sampling dates Continued 0 1 2 4 0 2 4 1 4 1 1 0 4 0 E ( 42 72 15-11 0 1 0 1 3 6 3 0 3 0 0 7 0 C 52 10 97 TABLE 4 TABLE 0 0 1 0 0 7 0 0 7 0 2 2 0 4 0 0 R 0 1 0 1 1 7 1 0 3 0 0 0 0 6 0 0 E 31-10 2 1 2 7 6 6 0 0 0 5 0 0 1 2 0 C 10 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 R exclusion barrier (E) and exclusion barrier and (R) removed (Number treatments per 9.2 m 0 0 0 0 0 0 0 0 0 0 1 5 1 0 0 0 E 16-10 0 0 0 0 0 1 0 0 0 0 0 2 0 0 0 0 C Effect of manipulating carabid abundance number on number in (C), control of untreated collected arthropods by D-Vac Carabid H YM ENOP T ER A HE M IP T ER A Muscidae Tipulidae Cecidomyiidae Sciaridae Mycetophilidae Chironomidae Phoridae Syrphidae Dolichopodidae Braconidae (Aphidiinae) Braconidae Chalcidoidea Other subfamilies Figitidae Proctotrupidae Nabidae

108 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (1): 101-111, March 2007 beetles, it is more probable that the first is a 0 0 R 77 more possible explanation. The number of noctuid larvae did not show 0 0 E statistical differences between exclusion plots 57 30-01 and controls, despite the higher presence of C. vagans inside the unexcluded crops. Yet, 0 1 C 72 some species of this genus have been used in programmes of biological control (Burgess and 2 1 R 71 Collins 1915). This situation suggest that the methodology of exclusion barriers, may be an 2 2 E 26 unappropiate method for insects able to move 26-12

) actively but unable to surpass polythene barri- 2

5 2 ers, since there is a constant replenishment of C 61 new insects (larvae) from the surrounding area in control plots, a situation that does not occur 0 0 R 36* in exclusion plots. In addition, operating pitfall traps continuously in exclusion and removal 1 1 E 12

2-12 plots, can catch a large number of noctuid larvae, such as occured in this experiment (Table 2) and 0 9 0 C may be the mechanism responsible for supress its numbers; therefore, the lack of an effective ) regulation of noctuid larvae by carabids may be 1 0 R 11

Sampling dates an artefact of the methodology employed. The large increase in the number of spring- Continued 0 8 0 E (

15-11 tails in the exclusion and removal treatment in relation to the other two treatments, could have 0 9 0 C occured through two different processes, act- TABLE 4 TABLE ing independently or in a complementary way. 0 5 0 R The removal of carabids may have reduced the predatory pressure on springtails, allowing an increase in their number, since some species 0 3 0 E

31-10 of carabids are important predators of these insects. On the other hand, because carabids 0 8 0 C are polyphagous predators, they could supress other springtail antagonists, such as arachnids 0 6 0 R (Dinter 1998, Sunderland et al. 1994) and

exclusion barrier (E) and exclusion barrier and (R) removed (Number treatments per 9.2 m through this mechanism, increase the number

0 1 0 of springtails. This may also be the case for E

16-10 agromyzid adults: An increase in the number of arachnids during one of the sampling dates 0 6 0 C Effect of manipulating carabid abundance number on number in (C), control of untreated collected arthropods by D-Vac in plots with exclusion and removal may be related to the predatory action of carabids on arachnids (mites excluded). The study shows that the effect of polyphagous opportunistic predators, such as carabid beetles, on the inver- T HROPODS 1

Carabid tebrate fauna of ecosystems can be extremely complex. Due to their wide range of prey, they can interact with plant-invertebrate food webs, T H Y S A NOP ER A R O T HER Arachnids Chilopods Significantly * P≤0.05 1 Mites are excluded.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (1): 101-111, March 2007 109 feeding at several trophic levels simultane- REFERENCES ously. There are many cases in the literature on the effect of insectivorous birds feeding at Blackman, R. & E. Eastop. 1985. Aphids on the world’s different trophic levels, which can increase pest crops. An Identification Guide. John Wiley, Chichester, England. 466 p. populations, when the effect predator suppre- sion is greater than the direct mortality caused Burgess, A.F. & C.W. Collins. 1915. The Calosoma beetle on the pest (cascade effect) (Tscharntke 1977). (Calosoma sycophanta): in New England. US Dept. Invertebrate predators preying at different tro- Agric. Bull. 251. 40 p. phic levels have been less studied, but there are Carrillo, R. & E. Zúñiga. 1974. Key to identify aphids also examples of how a predator can interfere (Homoptera: Aphididae) infesting cereal crops in with other predators through intraguild pre- Chile. Agro Sur 2: 86-87. dation and then indirectly cause an increase Coaker, T.H. 1965. Further experiments on the effect of of the prey (Press et al. 1974, Rosenhein et beetle predators on the numbers of the cabbage root al.1995). In summary the number and diversity fly, Erioischia brassicae (Bouché), attacking brassica of polyphagous predators can play an important crops. Ann. Appl. Biol. 56: 7-20. role in affecting the population stability of phy- Dinter, A. 1998. Intraguild predation between erigonid spi- tophagous insects. ders, lacewing larvae and carabids. J. Appl. Entomol. 122: 163-167.

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