BioControl DOI 10.1007/s10526-011-9425-z Impact of predatory carabids on below- and above-ground pests and yield in strawberry Jana C. Lee • David L. Edwards Received: 23 June 2011 / Accepted: 10 November 2011 Ó International Organization for Biological Control (outside the USA) 2011 Abstract The impact of adult carabid beetles on placed on the soil surface in the first year. Decreasing below- and above-ground pests and fruit yield was carabid density within exclusion plots resulted in examined in the laboratory and a two-year strawberry fewer marketable fruits compared to control plots in field study. In the laboratory, adults of Carabus both years. These results suggest that certain adult nemoralis Muller, Nebria brevicollis (F.), Pterosti- carabids may have limited impact belowground, and chus algidus LeConte, Pterostichus melanarius (Illig- some beneficial impacts above-ground with pest er), and Scaphinotus marginatus Fischer (Coleoptera: control and crop protection. Carabidae) consumed black vine weevil, Otiorhyn- chus sulcatus (F.) (Coleoptera: Curculionidae) eggs, Keywords Carabidae Á Density-manipulation plots Á larvae and/or pupae placed on the surface. The same Otiorhynchus sulcatus Á Pterostichus melanarius Á five carabid species showed no impact or low removal Weed seed predation rates of O. sulcatus larvae that had burrowed into the root of potted strawberry plants. In an assay with only P. melanarius, adults consumed O. sulcatus larvae placed on the soil surface more frequently than larvae Introduction buried 1.3 or 5 cm below. In a field study, the density of adult carabids, predominantly P. melanarius, was Carabid beetles are common polyphagous predators, manipulated with augmented, exclusion, and open and a review of 241 species of adult carabids from 110 control plots (2 9 2 m). Manipulating carabid density studies reveals that pest Lepidoptera were killed by had no impact on the removal of sentinel O. sulcatus 43% of carabid species, Diptera by 20%, Coleoptera larvae and pupae that were buried belowground which by 12% and Homoptera by 12% of species examined is consistent with laboratory observations. Increasing (Sunderland 2002). Also, ten genera of carabids are carabid density within augmented plots led to greater known seed predators in North America (Tooley removal of red clover seeds, Trifolium pratense L., and Brust 2002). Adult carabids frequently burrow beneath the soil during parts of the day and could potentially suppress pests belowground. While a Handling Editor: Patrick De Clercq wealth of studies exist on carabid predation, fewer studies have focused on belowground predation by & J. C. Lee ( ) Á D. L. Edwards adult carabids. Numerous predation studies of dipteran USDA ARS, Horticultural Crops Research Laboratory, 3420 NW Orchard Avenue, Corvallis, OR 97330, USA and coleopteran pests focus on the egg or larval pest e-mail: [email protected] stages that occur on the soil surface or above, or the 123 J. C. Lee, D. L. Edwards removal of sentinel pests placed on the surface study were: (1) to confirm predation of adult carabids (Sunderland 2002). on O. sulcatus in the laboratory, and (2) to evaluate Potential evidence of belowground predation by the impacts carabid adults have on belowground carabid adults includes studies that use belowground O. sulcatus larvae and pupae, above-ground weed sentinel prey, predator gut content analysis, or seeds, and fruit harvest in strawberry fields. Red manipulating predator densities. Two carabid species clover, Trifolium pratense L., is a common perennial have been shown to substantially remove sentinel weed and the seeds were used in this study because weed seeds buried 0.5 or 1.0 cm below in greenhouse they might be encountered by carabids foraging in experiments (White et al. 2007). DNA analysis of strawberry fields in the Pacific Northwest. adult carabids collected from citrus orchards (Monzo´ et al. 2011), and immuno-analysis of carabids from wheat fields (Floate et al. 1990) indicated that carabids Methods were consuming a fruit fly and midge pest, respec- tively. When carabids were excluded from oilseed Laboratory experiments rape plots, the number of emerging adult weevils from the soil was higher than from plots accessible Potential predation was monitored in a simple arena to carabids (Zaller et al. 2009). Conversely, when using field-collected carabids of five species: Carabus carabids were augmented to plots, the number of nemoralis Muller, Nebria brevicollis (F.), Pterosti- emerging adult pollen beetles from the soil was chus algidus LeConte, Pterostichus melanarius (Illig- marginally reduced (Zaller et al. 2009). It is important er), and Scaphinotus marginatus Fischer (Coleoptera: to consider that the examples cited (Floate et al. 1990, Carabidae). Individual carabids were starved with Zaller et al. 2009, Monzo´ et al. 2011) may also reflect water for 24 h and given either 50 O. sulcatus eggs on carabids encountering pest larvae at the soil surface as wet filter paper in a 14 cm diameter Petri dish, or ten the pest moves from the plant into the soil to pupate. O. sulcatus 5th instar larvae or five pupae placed on Strawberries are a high-value crop grown world- top of 4 mm of moistened sieved loam in a 0.59 l wide in temperate areas, and plagued by aphids, mites, plastic container. All carabid species were tested for root weevils, slugs and weeds. A review of biological consumption of O. sulcatus larvae, but only some control in strawberries describes carabids contributing species for consumption of eggs and pupae depending to vine weevil and slug control (Cross et al. 2001). on availability. The number of prey consumed was Root weevils including black vine weevil, Otiorhyn- checked after 24 h. In a second study, predation of chus sulcatus (F.) (Coleoptera: Curculionidae), are O. sulcatus larvae by adult carabids of the same five very damaging because the larval stage feeds on species was monitored in infested potted strawberry strawberry roots and diminishes plant growth. plants. A strawberry plant in a 3.8 l pot was inoculated Management of weevils in strawberries often relies with ten O. sulcatus fourth-instar larvae one week on chemical treatments with limited biological control prior to experimentation. This allowed pest larvae to options (DeFrancesco et al. 2002). Trench barriers burrow, feed, and establish before introduction of have shown to protect strawberries from immigrating carabids. One adult carabid or none (control) was weevils but can also stop the immigration of beneficial placed per strawberry plant and prevented from carabids and can be costly to implement (Bomford and escape by enclosing the upper part of the pot in a Vernon 2005). 30 9 30 9 30 cm Bug Dorm (BioQuip, Rancho The effectiveness of carabids in controlling O. Dominguez, California, USA). After one week of sulcatus requires further study. Carabids of unknown exposure, the soil from the strawberry plants was species were described to consume O. sulcatus eggs removed to count the number of surviving O. sulcatus and larvae in the laboratory (Evenhuis 1983; Garth and larvae. A t-test with the control determined whether Shanks 1978). Evidence of O. sulcatus predation in the each carabid species significantly reduced the propor- field was anecdotal. Insecticide-treated plots had more tion of O. sulcatus larvae recovered from the pot O. sulcatus and fewer carabids suggesting that the lack (arcsine-transformed). In a third study, only P. melana- of carabids and predation activity led to higher pest rius were used due to availability. Starved adults were abundance (Evenhuis 1982). The objectives of this placed separately into 2.4 l containers with 7.6 cm of 123 Carbid predation in strawberry loam, and five O. sulcatus 4–5th instar larvae that were: same augmented and control plots, and removed from (1) placed on the surface, (2) buried 1.3 cm below, or (3) exclusion plots. Trapping occured from 14 July to 30 5 cm below. Larvae were counted after 24 h. A Pear- October in 2008, and from 7 May to 1 October in 2009, son’s v2 analysis tested for the effect of depth on the and then every other week 12–29 October in 2009. presence or absence of predation, and an ANOVA tested After manipulating carabid densities, predation was the effect of depth on the proportion of larvae consumed monitored with sentinel O. sulcatus larvae and pupae, (arcsine-transformed). and red clover seeds, T. pratense. For larval predation, two strawberry plants were randomly selected per plot Field experiments for infestation. Ten lab-reared 5th instar O. sulcatus were inoculated per plant. After 20–28 days, inocu- A 0.134 and 0.036 ha field of ‘Hood’ strawberries lated plants were dug up and carefully screened for were planted on 12–13 May 2008. No insecticides surviving larvae. Surviving larvae were expected to were used in the fields, but manual weeding and her- remain in the larval stage because the 5th instar bicide applications of Poast (sethoxydim), Roundup develops for 119–115 days, and the 6th instar devel- (glyphosate), Stinger (clopyralid), Spartan 4F (sulf- ops for 130–211 days before pupating (La Lone and entrazone), and Aim (carfentrazone) were done in Clarke 1981). New replacement strawberry plants 2008–2009. To determine the role of carabids in were immediately transplanted into plots. Larval weevil control, carabid densities were manipulated in predation tests were conducted when larger O. sulc- small enclosed ‘augmented’ and ‘exclusion’ plots, and atus larvae would be expected in the field: 18 July–15 unenclosed control plots. Barriers used to manipulate August, 21 August–17 September, 1–23 October in predator densities provide an effective test of whether 2008, 28 July–17 August, 19 August–8 September, carabids can have an impact on pest levels (Menalled and 17 September–7 October in 2009. For pupal et al. 1999; Sunderland 2002). Plots were 2 9 2min predation, seven lab-reared O.