Do Turning Biases by The 7spot Ladybird Increase Their Foraging Efficiency

Do Turning Biases by the 7-Spot Ladybird, Coccinella septempunctata, Increase Their Foraging Efficiency? Author(s): Robbie D.
Girling, Mark Hassall and John G. Turner Source: Behaviour, Vol. 144, No. 2 (Feb., 2007), pp. 143-163 Published by: BRILL Stable URL: http://www.jstor.org/stable/4536437 . Accessed: 06/08/2013 11:03
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Do turning biases by the 7-spot ladybird, Coccinella increase their foraging efficiency? septempunctata,
Robbie D. Girling"2'3),Mark Hassall') & John G. ITrner4)

School of Environmental Sciences, (1 Centrefor Ecology, Evolutionand Conservation, Universityof East Anglia, Norwich NR4 7TJ, UK; 4 School of Biological Sciences, Universityof East Anglia, Norwich NR4 7TJ, UK) (Accepted:21 December2006)
Summary L. would exhibit a The hypothesisthatforagingmale and female Coccinella septempunctata turningbias when walking along a branchedlinear wire in a Y-mazewas tested. Individuals were placed repeatedlyin the maze. Approximately45% of all individualstested displayed significantturningbiases, with a similarnumberof individualsbiased to the left and right.In the maze right-handed individualsturnedrightat 84.4%of turnsand the left-handedindividuals turnedleft at 80.2% of turns.A model of the searchingefficiency of C. septempunctata in dichotomousbranchedenvironmentsshowed that model coccinellids with greaterturning of the plant for a given numberof searchesthanthose biases discovereda higher proportion with no bias. A modificationof the model to investigateforaging efficiency, by calculating the mean time taken by individualsto find randomlydistributedaphid patches, suggested thaton four differentsizes of plants, with a varietyof aphidpatch densities, implementinga turningbias was a significantlymore efficient foraging strategythan no bias. In general the benefits to foraging of implementinga turningbias increasedwith the degree of the bias. It to have a turning may be beneficialfor individualsin highly complex branchedenvironments bias slightly lower than 100%in orderto benefitfrom increasedforagingefficiency without walking in circles. Foragingbias benefits increasedwith increasingplant size and decreasing aphid density. In comparisonsof two differentplant morphologies,one with a straight stem and side branchesand one with a symmetricallybranchedmorphology,there were few significantdifferences in the effects of turningbiases on foraging efficiency between morphologies.
2) Corresponding author'se-mail address:robbie_girling@hotmail.com 3) Correspondingauthor'scurrentaddress: 13 EastmeadLane, Stoke Bishop, Bristol BS9 lHW, UK
o KoninklijkeBrill NV, Leiden, 2007
Behaviour144, 143-163 Also availableonline - www.brill.nl/beh
144
Girling,Hassall & Turner
Keywords:cropping strategy, outline tracing, handedness, foraging efficiency simulation model.
Introduction insects use a numberof differentforagingpatternsin orderto opPredatory timise theirpatch discoveryrate. Searchorientationcan be divided into two phases, searchstrategiesand searchtactics. A searchstrategyis 'a set of basic rulesof scanningandlocomotionthatresultsin the effective encountering of food'. A search tactic is 'an adaptivechange in of a specific distribution scanning or locomotion occurringonce a predatorhas arrivedin a specific areawhere prey are available'(Smith, 1974). in geometrically Insects typically searchfor food, hosts or sexual partners complex environments(Casas & Aluja, 1997), for example, aphidophagous coccinellids often oviposit, and feed on aphids, on a wide range of plant species (Majerus& Kearns, 1989). The majorityof studies of foraging behaviourof coccinellids have been conductedon their larvae (Dixon, 2000); however, Kindlmann& Dixon (1999) suggest that the search strategiesof adult coccinellids selecting suitablepatches for oviposition are likely to be the most influentialin determiningthe animal'sfitness. When a coccinellid is in a branchedplant environmentselection will favour individualsthat use the most efficient mechanismto find aphids on a plant. Physical cues and plant architecture can greatly effect coccinellid foraging, for example a greater degree of overlap between leaves of adjacent plants greatly increases the rate at which adult convergentladybird beetles Hippodamiaconvergens,move throughvegetation(Kareiva& Perry, 1989). In experimentsmonitoringthe movement of C. septempunctata,in different sized plots of broccoli, the spatial scale of plots and occurrence of patch boundariesmodified individuals' displacementand movementbehaviour(Banks & Yasenak,2003). Additionally,C. septempunctata displays area restrictedsearch behaviourfollowing the consumptionof aphids, by increasing the frequency at which they turn (Nakamuta,1985). This area restrictedsearching results in aggregationof predators(Karieva& Odell, 1987). Some coccinellids can only detect aphidsvisually at very shortdistances; 7 mm in adultC. septempunctata (Nakamuta,1984). Thereis some evidence to suggest thatcoccinellids are able to use aphidvolatiles as cues to findtheir
Turning biases by C. septempunctata
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prey (Obata, 1986; Raymondet al., 2000; Sengonca & Liu, 1994), although other authorssuggest that coccinellids are not able to detect volatiles from aphids alone (Nakamuta,1984; Schaller & Nentwig, 2000; Ninkovic et al., 2001; Girling & Hassall, unpubl.), as is the case for the larvae of Adalia bipunctata,which are not attracted by the odourof aphids(Hemptinneet al., 2000). In a comprehensivereview, Dixon (2000) concluded that we do not know the extent to which olfactoryand visual cues are used by coccinellids to search for prey, but that when they are used they can only detect such cues over shortdistances.Therefore,therewill be strongselection to evolve the most efficient basic rules for locomotion to maximise the probabilityof encountering prey patches. One such search strategy is 'cropping'. This is often used by animals that need to locate many food objects (Jander,1977). Some ants search horizontalbranchesusing a cropping strategyknown as 'outline tracing'. When searchingon a branchan ant will make either a right or a left turn and will continue to turnin the same directionat every following junction it encounterson the branch.This ensures that the overall path length will be as shortas possible (Jander,1977). Outlinetracingis based on an insect showing an innatebias to turnin one directionor another,often referredto as 'handedness'. Many experiments on insect foraging behaviour have been conducted in Y-tube olfactometers.In these types of experiments,any evidence that the insect is using a searching strategy of outline tracing would result in invalidationof the commonly assumed null hypothesis that the insect will follow each branchof the olfactometer50% of the time. The present study was designed to investigate possible turning biases in a population of C. septempunctataon a stylised branch in a Y-tube olfactometer with no odour sources in either arm, i.e., a Y-maze. A simulationmodel was used to investigate whether turningmore frequentlyin one direction would increasesearchingefficiency of an individualin a branchingenvironment. The specific hypotheses tested were: 1. Individualmale and female C. will show significantturningbiases when walkingon a stylseptempunctata ised branch in a Y-maze, which was tested with laboratoryexperiments; and 2. Turningbiases will alter the searchingefficiencies of individualcoccinellids foraging in complex branchingenvironments,which was tested with a simulationmodel.
Turningbiases by C. septempunctata
147
Figure 1. Details of design of PerspexY-maze.
Air, without any volatiles introduced,was pumped throughan activated charcoalfilter,throughTeflontubingand dividedin two by a T-junction. The two airfiowsthen passed throughseparateflow meters, which regulatedthe flow rate at 400 ml min-'. The air then passed into the arms of the Y-maze. All experimentswere conductedin a constanttemperature room at ca. 230C. The majorityof previous studies using Y-tube olfactometershave oriented them horizontally,e.g., Steinberget al. (1992). Therefore,the Y-mazein this study was also oriented horizontally,so that the results could be directly comparableto those of previous studies. The Y-maze was lit from above by a fluorescentlamp, fittedwith a prismaticfilter,to ensure a completely even light distribution. Laboratorytestfor bias in individualC. septempunctata Individualswere placed one at a time on the wire at the stem end of the maze and given 5 minutes to enter either arm.When an individualenteredone of the armsof the maze it was recordedas havingmade a turningdecision. After each individualcoccinellid was tested, the maze was dismantled,cleaned with tissue soaked in 100%ethanol and allowed to dry before the next test. For each individual several different linear wires were selected randomly to avoid any consistent physical asymmetryin the simulatedbranch.Each individualwas testedbetween 14 and 16 times, aligningthe maze to different points of the compass an equal numberof times to negate the effects of any environmental gradientswithin the room. Each individualwas tested at each
148
compass point on more than one day to eliminate any randomdaily bias. 24 hoursbefore testing. Starving Individualswere starvedfor approximately beetles for 18 hours resultedin maximumsearchactivity (Frazer& Gilbert, 1976). A total of 42 individuals were tested: 17 male and 25 female. For each individualtested, the total numberof left and right turningdecisions was comparedusing a chi-squaretest. Simulationmodel of searching in branchedenvironments A simple model was developed,using MicrosoftVisual Basic 6.0' software, to investigatehow turningbiases affect the searchingefficiencyof C. septemThe model was used to inpunctatain dichotomousbranchedenvironments. vestigatethe effect of turningbias on the rateat which a plant was explored. It was assumed that no other stimuli were used in searching.Searchingbehaviourwas simulatedfor two differentbranchmorphologies:i) a symmetrically branchedplant(Figure2a); and ii) a plantwith a straightstem and side branches(Figure 2b). Four sizes of plants were used, with 7, 15, 31 and 63 branches,these numbersbeing derivedby addingan extralayer of branches to the basic seven-branch symmetricalplantfor each incrementof size. The model was based on the following rules: individuals 1) always start searching at the base of a plant; 2) always walk at the same speed along equal length branches;3) walk in the same direction along a branchuntil they reach the end of it when they turnaround(Frazer& McGregor(1994) demonstratedon leaf models that C. septempunctatamost often left the leaf model by turningaroundand walking back down the stem); 4) when
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biases by C. septempunctata Turning
149
reachinga junction always have to 'select' to turneither left or right, with a frequencydeterminedby the turningbias with which the individualwas programmed. The responsesof individualswith threedifferentturningbiases were investigated:i) 50% left-turns(no bias, i.e., at each junctiontherewas a 50%probabilityof the individualturningleft or right);ii) 80%left-turning bias (the meanleft-turning bias of the individualsthatwere significantlyleftiii) 100%left-turning bias. Each movement handedin the maze experiment); an individualmade from one branchto anotherwas counted as one unit of search. Discovery of a branchwas defined as the first time an individual walked on it. The percentageof the plant discovered was determinedfor different lengths of search, that is, for different numbersof search units, e.g., 5, 10, 25, 50, 100 up to 1000 in a search. Each length of search was run 100 times, simulatingthe responses of 100 individualsand responses averagedto give the mean searchefficiency,definedas the mean percentage of the entireplantdiscoveredfor a given searchlength. Additionally,a modificationto the model was made to investigatethe effects of turningbias' on foragingefficiency,by calculatingthe mean number of searchesrequiredfor modelled individualsto locate differentnumbersof randomlydistributed aphidfood patches.Aphid patcheswere randomlyassigned to one of the plants branches(other than the startingbasal branch), each branchcould only be assigned one patch,and discoveryof a patchwas defined as the first time an individualwalked on that branchassigned with a patch. The mean numberof searchunits requiredfor 500 simulatedcoccinellid individualsto discover an aphidpatch was determined,for each of the 50%, 80%and 100%turningbias categories,at the following aphidpatch densities:(a) One aphidpatchrandomlylocated on any branchof the plant, for each of the four plant sizes, of both plant morphologies;and (b) Multiple aphid patches randomlylocated, on both plant morphologiesof only the 63 branchplants, with either 3, 6, 9 or 16 branchespossessing an aphid patch (this correspondsto aphid patch densities of ca. 5, 10, 15 and 25% of branches,respectively).These densities were chosen because aphidnumbers in naturefluctuategreatly(dependingon the season, stage of infestation etc.) (Dixon, 1998) and at high aphid densities, the difference in foraging efficiencybetween an individualusing a foragingstrategyandone searching at randomwill likely be reduced,assumingthat the aphid patches are ranon the plant.For example, if aphiddensities reach >25% domly distributed (i.e., morethanone branchin fourinfested),thenit is unlikelythata foraging
151
Table 1. Numberof turnsmade by individualmale and female C. septempunctata when repeatedlytested in a Y-maze.
% % No. of Individual No. of x2 Number left turns rightturns left turns rightturns 1 2 3 4 5 6 7 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 37 38 39 40 41 42 13 13 13 12 12 12 12 12 12 12 11 11 10 10 9 9 9 9 8 8 8 8 8 7 7 7 6 6 6 6 5 5 4 4 4 3 3 3 2 2 1 0 1 3 3 2 2 4 4 4 4 4 5 5 4 6 5 7 7 7 6 6 8 8 8 9 9 9 8 8 10 10 9 11 10 12 12 13 13 13 12 14 13 16 92.9 81.25 81.25 85.7 85.7 75 75 75 75 75 68.75 68.75 71.4 62.5 64.3 56.25 56.25 56.25 57.1 57.1 50 50 50 43.75 43.75 43.75 42.9 42.9 37.5 37.5 35.7 31.25 28.6 25 25 18.75 18.75 18.75 14.3 12.5 7.1 0 7.1 18.75 18.75 14.3 14.3 25 25 25 25 25 31.25 31.25 28.6 37.5 35.7 43.75 43.75 43.75 42.9 42.9 50 50 50 56.25 56.25 56.25 57.1 57.1 62.5 62.5 64.3 68.75 71.4 75 75 81.25 81.25 81.25 85.7 87.5 92.9 100 p Handedness Left Left Left Left Left Left Left Left Left Left Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Ambidextrous Right Right Right Right Right Right Right Right Right Sex y
10.29 <0.01 6.25 0.01 6.25 0.01 7.14 0.01 7.14 0.01 4 0.05 4 0.05 4 0.05 4 0.05 4 0.05 2.25 0.13 2.25 0.13 2.57 0.11 1 0.32 1.14 0.29 0.25 0.62 0.25 0.62 0.25 0.62 0.29 0.59 0.29 0.59 1 0 1 0 1 0 0.25 0.62 0.25 0.62 0.25 0.62 0.29 0.59 0.29 0.59 0.32 1 1 0.32 1.14 0.29 2.25 0.13 2.57 0.11 4 0.05 4 0.05 6.25 0.01 6.25 0.01 6.25 0.01 7.14 0.01 <0.01 9 10.29 <0.01 <0.001 16
y c
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154
Table 2. Results of Mann-Whitneytests, used to analyse simulationdata, comparingthe mean numberof searchestaken to discover a randomlydistributedaphid patch, by simulated coccinellids programmedwith one of three different turningbiases, between pairs of different turningbias categories, within each of eight plant morphology and plant branch number combinations.
Turningbias categories 7 50% vs. 80% Z -2.28 p 0.02 Symmetricalplant size (# branches) 15 -1.96 0.05 31 63 7 Straightplant size (# branches) 15 -2.48 0.01 31 63
-3.60 -2.09 -4.28 0.04 <0.001 <0.001
-4.93 -3.55 <0.001 <0.001
-7.26 -11.97 -15.42 -4.30 -6.21 -7.79 -11.16 50% vs. 100% Z -4.56 p <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 80% vs. 100% Z -2.12 0.03 p -4.61 -3.06 <0.001 <0.01 -7.81 -2.12 0.03 <0.001 -8.77 -11.68 -4.98 <0.001 <0.001 <0.001
increasedso did the level of significanceof comparisonsof the meannumber of searches taken to find a patch between differentturningbias categories (Table 2). This indicates that the foraging benefits of employing a turning bias increasewith increasingplant size. In comparisonsbetween the two plant morphologies,of the mean number of searchestakento discover the aphidpatch by simulatedcoccinellids, for pairsof matchingturningbias categorieswithin each plant size, the only significantdifferences between morphologieswere in the 100% bias category on the 31 (M-W, Z = -6.50, p < 0.001) and 63 (M-W, Z = -4.67, p < 0.001) branchplants,where there were significantlyfewer searcheson straightplants, and in the 50% (M-W, Z = -3.59, p < 0.001) and 80% (M-W, Z = -2.00, p = 0.05) bias categories on the 63 branchplants, where therewere significantlyfewer searcheson symmetricalplants (Figure 3c & d). This suggests that there were very few differencesin foragingefficiency between the two plant morphologies,for all turningbias categories, except at largerplant sizes where a 100%bias was more efficient on straight than symmetricalplants, and no bias or an 80% bias was more efficient on symmetricalthanstraightplants.
Turning biasesby C. septempunctata
155
Simulationresults:Modellingforaging on 63 branchplants with multiple aphidpatches aphid On simulated63 branchplants,assignedmultiplerandomlydistributed patches, there were significantdifferencesin the mean numberof searches with takento discoveran aphidpatch,by simulatedcoccinellidsprogrammed differentturningbiases, between all turningbias categories,on symmetrical 0.001), branchingplants with: 3 patches (K-W, x2 = 38.4, df = 2, p < 6 patches (K-W, x2 = 8.2, df = 2, p = 0.02), 9 patches (K-W, x2 = 6.8,
df = 2, p = 0.03), but not 16 patches (K-W, x2 = 5.0, df = 2, p = 0.08)
(Figure4a); and also on all straightbranchingplants with: 3 patches(K-W,

X2 = 98.7, df = 2, p < 0.001), 6 patches (K-W, x2 = 35.1, df = 2,
0.001), 16 patches(Kp < 0.001), 9 patches(K-W,x2 = 26.9, df = 2, p < in comparisons 0.001) (Figure4b). Furthermore, W, x2 = 18.4, df = 2, p < of the mean numberof searches taken to discover an aphid patch between individualpairs of differentturningbias categories,within each of the eight plantmorphologyand aphidpatch density combinations,all pairs were sig0.05, except for comparisonsbetween the nificantlydifferentto at least p < 50% and 80% bias categorieson symmetricalplants with 16 aphidpatches, and the 80% and 100%bias categorieson symmetricalplants with 6, 9 and 16 aphidpatches(Table3). In all comparisons,regardlessof whetherdifferwith a 100%turning ences were significantor not, coccinellids programmed with bias took the fewest mean numberof searchesand those programmed no bias took the greatest.These data suggest that implementinga turning bias was a significantlymore efficient foraging strategythan implementing no turningbias at all aphiddensities on both plantmorphologies,except for the 80% bias category on the highest level of aphid patch density on symon symmetricallybranchedplants possessing metricalplants. Furthermore, the three highest aphid patch densities there was no significantincrease in foragingefficiency for coccinelids implementinga 100%turningbias over an 80% bias. These data also show a trend,althoughnot strictlyadheredto, that as aphid patch densities decreasedthe significanceof comparisonsof the mean numberof searchestakento find a patchbetween differentturning bias categories,increased(Table3). This indicatesthatthe foragingbenefits of employinga turningbias increasewith loweringaphiddensity. In comparisonsbetween the two plantmorphologies,of the meannumber of searches taken to discover the aphid patch by simulated coccinellids,
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Table 3. Results of Mann-Whitneytests, used to analyse simulationdata, comparing the mean number of searches taken to discover a randomly distributedaphid patch, by simulated coccinellids programmedwith one of three different turning biases, between pairs of different turning bias categories, within each of eight plant morphology and aphid patch number combinations.
Turningbias categories 3 50% vs. 80% Z p 50% vs. 100% Z p 80% vs. 100% Z p Symmetricalplant size (No. of aphidpatches) 6 9 16 3 Straightplant size (No. of aphidpatches) 6 -2.08 0.04 -5.74 <0.001 -3.92 <0.001 9 -2.87 <0.01 -5.22 <0.001 -2.21 0.03 16 -2.10 0.04 -4.29 <0.001 -2.21 0.03
-4.33 -2.56 -2.38 -1.12 -2.14 0.02 0.26 <0.001 0.03 0.01 -2.32 -2.12 -2.25 -10.06 -6.04 0.03 0.02 <0.001 <0.001 0.02 -5.31 -4.07 -0.61 -0.33 -1.10 0.27 <0.001 0.74 <0.001 0.54
for pairs of matching turning bias categories within each plant size, the only significantdifferences between morphologies were in the 100% bias category on plants with 3 (M-W, Z = -2.39, p = 0.02) and 6 (M-W, Z = -2.34, p = 0.02) aphidpatches, where there were significantlyfewer searcheson straight plants,andalso in the 50%bias categoryon plantswith 3
(M-W, Z = -2.43, p = 0.02) and 16 (M-W, Z = -2.31, p = 0.02) aphid
patches and the 80% bias category on plants with 6 (M-W, Z = -2.37, p = 0.02) aphid patches, where there were significantly fewer searches on symmetricalplants (Figure4). These results suggest that there were few differencesin foragingefficiency between plantmorphologiesbut thatat the two lower aphiddensities, implementinga 100%bias was more efficient on straightthan symmetricalplants.Additionally,on the occasions when the 50 and 80% biases were significantlymore efficient on one plant morphology thananotherit was always on the symmetricalbranchingplants.
Discussion We found thatnearlyhalf of both male andfemale C. septempunctata exhibited turningbiases when they encountereda single Y-junction(Table 1). On average left-handedindividualsmade 80.2% of turns to the left and righthanded individuals84.4% of turns to the right. Previously handednesshas
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Figure 4. Simulationmodel resultsof the mean numberof searchunits (durationof search) taken to discover randomlylocated aphid patches on a 63 branchedplant, at four different aphiddensities (3, 6, 9 and 16 aphidpatchesper plant),by individualswith threedifferentleft turningbiases (500 individualsper turningbias) on plants with: (a) symmetricalbranching morphology;and (b) straightbranchingmorphology.Bars markedby differentletters,within an aphidpatch density category,are significantlydifferent(Mann-Whitney, p < 0.05).
only been describedfor coccinellids in the unfed larvae of the 2-spot ladybird Adalia bipunctata(Banks, 1957), on flat surfaces. Bansch (1966) reportedno evidence of handednessin adults or larvaeof A. bipunctatawhen searchinga 50-cm-high branchingmodel tree, instead their behaviourwas suggested to be controlled mainly by geotaxis. C. septempunctatadid not displaya turningbias in a traditional glass Y-tubeolfactometerwithoutwires (Schaller& Nentwig, 2000). We suggest thatC. septempunctata behaveddifferentlywhen walking along branchedwires as these more closely resemble a branchedplant stem thandoes the surfaceof a glass tube. We have not yet tested whetherindividualsof C. septempunctata would respondsimilarlyon verticallyorientatedbranches. Other examples of turningbiases in arthropodsin Y-tube olfactometers and Y-mazeshave been reported.The tropicalantAzteca sp., walking along a wire in a Y-tubeolfactometershowed a similarturningbias (D. Edwards, pers. comm.) Turningbiases have also been reportedfor Aleochara bilieata (Coleoptera) (Putnam, 1962), Calcinus herbsteiiand Clibinariuszebra (two species of hermitcrab) (MacKay,1945, 1947) and Heliodrilus (Annel-
158
ida) (Swartz, 1929). There have also been a few reportsof turningbiases on flat surfaces,e.g., desert ants (Wehner& Srinivasan,1981) and Pediculus humanus(Anoplura)(Wigglesworth, 1941) and in other environments e.g. in a numberof bumblebeespecies (Cheverton,1982; Kells & Goulson, 2001). This suggests that turningbiases may be a widely distributedtrait, the Arthropoda. throughout However,the effects of turningbiases on foraging behaviourarelikely to be differentbetweendifferentfeeding guilds, e.g., predators,seed predators, herbivores,etc. The existence of biases in turningbehaviourof C. septempunctata, complicates the use of linearwire Y-tubeolfactometryas a bioassaybecausenull hypotheses have to be adjustedafter testing for handednessof each individual used. Using a linear wire howeverhas the advantageof more closely resemblingthe field environment, wherecoccinellids foragein a complicated three-dimensional matrix not only on flat surfaces(Casas& Aluja, branching 1997). The model of searchingefficiency suggests thaton all plant sizes of both plantmorphologies,model coccinellids with strongerturningbiases discovered a higher proportionof the plant for a given numberof searches than for those with no bias (50% left turns), thereforeturningbiases increased searchingefficiency (Figure3a & b). A modificationto the model to investigate the effects of turningbiases on foragingefficiency suggestedthaton all plantsizes of bothplantmorphologies,with a varietyof differentaphidpatch densities, implementinga turningbias was a significantlymore efficientforaging strategythan no turningbias (Figures 3 & 4). In general,the benefits to foragingefficiency of employingturningbiases increasedwith the degree of the bias. The model also suggestedthatthe benefitsof implementinga turningbias increasedwith increasingplantsize andalso increasedwith decreasingaphid density, i.e., the more scarce the aphid patches were, the greaterwere the increases in foraging efficiency. Because the averagedevelopmenttime of coccinellid larvaeis similarto the averagedurationof existence of an aphid prey patch,adultfemale coccinellids must find preypatchesto lay eggs in at an early stage in their development,to allow enough time for their larvaeto completetheirdevelopmentbeforethe aphidpatchdisappears (Hemptinne& Dixon, 1991). Therefore,becausethe model suggeststhatturningbiases may increaseforagingefficiency when aphidprey are scarce, turningbiases may increasean individualsprobabilityof discoveringsmallerprey patchesearly
160
while the larvae of the 14-spot ladybird,Propylea quatuordecimpunctata et al., 1984), have (Banks, 1957) andthe larvaeof C. septempunctata (Carter also been shown to search the edges of leaves. By following the principles of 'outline tracing', if individualsdisplay turningbiases they could benefit by increasingtheir foraging efficiency,as predictedby this model. Handedness on branches,combined with following the edges of small leaves and veins of largerones would, therefore,result in an effective cropping strategy. However althoughturningbiases may provide a foraging benefit they were not displayedby all individuals.There is a possibility that if handedwith ness is a geneticallyinheritedtraitit may be in a linkagedisequilibrium anothertrait,selection for which may influencethe presence of handedness within an individual.In the field manyfactorsaffect the foragingefficiencies of naturalenemies on plants. For example, it has been shown that a number of aphidpredators andparasitoidsincludingcoccinellids, foragemore effectively, walk for longer, and fall less frequentlyon pea plants with reduced wax comparedto those with normalwax and also may be more efficient at reducing aphid densities on reducedwax plants in the field (Eigenbrodeet al., 1998; White & Eigenbrode,2000a, b; Rutledge & Eigenbrode,2003; Rutledge et al., 2003; Chang et al., 2004). Therefore,factors such as how efficiently a coccinellid can traversea plant may have effects on the effectiveness of employing a turningbias in the field. In conclusion, in laboratory experimentsnearlyhalf of the 42 C. septempunctata tested displayed turningbiases. Therefore,we used these data to create a model to investigatewhetherturningbiases could have an effect on foraging efficiency. From this, we predictthat turningbiases may result in selective advantagesin foragingefficiency if C. septempunctata employs an 'outline tracing' croppingstrategy,which would be most effective at lower aphid densities. The next stage of this researchis to test these predictions with ladybirdsforaging for aphids on real branchedplants and monitoring differencesin capturerates.
Acknowledgements We thank Prof. A.F.G. Dixon, Prof. G. Poppy, Dr. B. Emerson, Dr. W. Powell, Dr. D. Yu and two anonymousreferees for their comments, BrendanO'Brien for constructionof the Y-maze,David Alden for maintenanceof aphidculturesand PhilipJudgefor drawingthe figures. This work was fundedby a studentshipto Dr. R. Girlingfrom the NaturalEnvironment ResearchCouncil and a small ecological projectgrantfrom the BritishEcological Society.
Turningbiases by C. septempunctata References
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Do Turning Biases by The 7spot Ladybird Increase Their Foraging Efficiency

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Do Turning Biases by the 7-Spot Ladybird, Coccinella septempunctata, Increase Their Foraging Efficiency? Author(s): Robbie D.

Robbie D. Girling"2'3),Mark Hassall') & John G. ITrner4)

o KoninklijkeBrill NV, Leiden, 2007

Behaviour144, 143-163 Also availableonline - www.brill.nl/beh

Girling,Hassall & Turner

Keywords:cropping strategy, outline tracing, handedness, foraging efficiency simulation model.

Turning biases by C. septempunctata

Figure 1. Details of design of PerspexY-maze.

Girling,Hassall & Turner

moadelg plndcte mopdoifes:n (a)dsmmetual plant;hb)strih.pat Figure2.DSeven-ranch

biases by C. septempunctata Turning

y y e y y c? y y y y a' e a' o' o' y y y

Girling,Hassall & Turner

-3.60 -2.09 -4.28 0.04 <0.001 <0.001

-4.93 -3.55 <0.001 <0.001

Turning biasesby C. septempunctata

(Figure4a); and also on all straightbranchingplants with: 3 patches(K-W,

Girling,Hassall & Turner

(percentageof wholetree in parentee)

Girling,Hassall & Turner

Girling,Hassall & Turner

Turningbiases by C. septempunctata References

Girling,Hassall & Turner

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