Altruism during predation in an assassin bug

12 Pages·2017·0.69 MB·English

Altruism during predation in an assassin bug
Alain Dejean, Messika Revel, Frédéric Azémar, Olivier Roux
To cite this version:
AlainDejean,MessikaRevel,FrédéricAzémar,OlivierRoux. Altruismduringpredationinanassassin
bug. The Science of Nature Naturwissenschaften, 2013, vol. 100 (10), pp. 913-922. ￿10.1007/s00114-
013-1091-9￿. ￿hal-01091981￿
HAL Id: hal-01091981
https://hal.archives-ouvertes.fr/hal-01091981
Submitted on 8 Dec 2014
HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est
archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents
entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non,
lished or not. The documents may come from émanant des établissements d’enseignement et de
teaching and research institutions in France or recherche français ou étrangers, des laboratoires
abroad, or from public or private research centers. publics ou privés.
Open Archive Toulouse Archive Ouverte (OATAO)
OATAO is an open access repository that collects the work of Toulouse researchers and
makes it freely available over the web where possible.

This is an author-deposited version published in: http://oatao.univ-toulouse.fr/
Eprints ID: 11543

Identification number: DOI : 10.1007/s00114-013-1091-9
Official URL: http://dx.doi.org/10.1007/s00114-013-1091-9

To cite this version:
Dejean, Alain and Revel, Messika and Azémar, Frédéric and Roux, Olivier
Altruism during predation in an assassin bug. (2013) Naturwissenschaften, vol.
100 (n° 10). pp. 913-922. ISSN 0028-1042

Any correspondence concerning this service should be sent to the repository administrator:
[email protected]
Altruism during predation in an assassin bug
AlainDejean&MessikaRevel&FrédéricAzémar&
OlivierRoux
Abstract Zelusannulosus isanassassinbugspeciesmostly stickysubstanceofthesundewsetaeontheirforelegsaidsin
noted on Hirtella physophora, a myrmecophyte specifically prey capture. Group ambushing permits early instars tocap-
associatedwiththeantAllomerusdecemarticulatus knownto tureinsectsthattheythenshareornotdependingonpreysize
buildtrapsonhosttreetwigstoambushinsectpreys.TheZ. and the hunger of the successful nymphs. Fourth and fifth
annulosus females lay egg clutches protected by a sticky instars,withgreaterneeds,ratherambushsolitarilyondiffer-
substance. To avoid being trapped, the first three instars of ent host tree leaves, but attract siblings to share large preys.
nymphs remain grouped in a clutch beneath the leaves on Communalfeedingpermitsfasterpreyconsumption,enabling
whichtheyhatched,yetfromtimetotime,theyclimbontothe smallnymphstoreturnsoonertotheshelteroftheirleaves.By
uppersidetogroupambushpreys.Long-distancepreydetec- improvingtheregularityoffeedingforeachnymph,itlikely
tion permits these bugs to capture flying or jumping insects regulates nymphal development, synchronizing molting and
thatalightontheirleaves.LikesomeotherZelus species,the subsequentlylimitingcannibalism.
Keywords Conspecifictolerance .Predation .Preysharing .
Communicatedby:SvenThatje
Reduviidae .Zelusannulosus
A.Dejean(*)
ÉcologiedesForêtsdeGuyane,Campusagronomique,BP316,
97379Kouroucedex,France
e-mail:[email protected] Introduction
A.Dejean
Grouphuntingfollowedbyfoodsharingbringsfitnessbene-
UniversitédeToulouse;UPS,Ecolab,118routedeNarbonne,
fitstotheparticipantsthroughincreasedpercapitafoodintake
31062Toulouse,France
while minimizing the cost of capture. Indeed, in addition to
M.Revel avoidingpredation,preys are capturedmoreeffectivelywith
NationalResearchCouncilofCanada,6100RoyalmountAvenue,
lessriskofinjury.Thisisknowninsocialspiders(Settepani
Montreal,QuebecH4P2R2,Canada
etal.2013;YipandRayor2013)andsomeantspecies(Cerda
M.Revel andDejean2011)and,amongvertebrates,infishes(deWaal
CentreINRS,InstitutArmand-Frappier,UniversitéduQuébec, 2006),birds,cetaceans,otters,carnivorans,andchimpanzees
Laval,QuebecH7V1B7,Canada
(seethesynthesisinBaileyetal.2013).Harrishawkscoop-
eratively hunt and rear young (Coulson and Coulson 1995).
F.Azémar
CNRS,LaboratoireÉcologieFonctionnelleetEnvironnement Hyenas, Lycaon, wolves, and lions also redistribute food
(UMR-CNRS5245),31062Toulouse,France betweenadults(Baileyetal.2013),asdoeusocialinsects.
Delayedbenefitsfromfoodsharingoccurinvampirebats
F.Azémar
whichregularlyfailtoobtainblood,theironlyfood,anddie
UniversitédeToulouse;UPS,INP,Ecolab,118routedeNarbonne,
31062Toulouse,France after 70 h if starved. Unsuccessful individuals can receive
regurgitationsfromroost-mates,frequentlyrelatives.Yet, re-
O.Roux
ceiving regurgitations depends mostly on having previously
IRD;MaladiesInfectieusesetVecteurs,Ecologie,Génétique,
providedthehelperwithblood,resultingintheformationof
EvolutionetContrôle(UMR-IRD224),ÉquipeBEES,IRD01,BP
171,Bobo-Dioulasso,BurkinaFaso food-sharing groups characterized by mutual allogrooming
(CarterandWilkinson2013).Achimpanzeepossessingfood, decemarticulatus, shelter. Workers of this species build
particularly meat, can share it with close relatives or in re- gallery-shaped traps permitting them to capture preys 1,800
sponseto harassmentbybeggarsorobtain adelayedbenefit times their weight (Dejean et al. 2005, 2013; Grangier et al.
throughgroomingandformingcoalitionsaccordingtodom- 2008a).Allomerus workers toleratethe fragile Z. annulosus
inance(Silketal.2013).Altruisticmotivationforfoodsharing firstinstarnymphsontheirhostplants(thesenymphsarethus
existsinbonoboswhichsharetheirfoodwithastrangerrather protected from other ants) and, later, the relatively large last
than with a group mate, but do not give food if a social instar nymphs do not attack these ants (Revel et al. 2010).
interactionisimpossible(TanandHare2013). Although several authors have provided information on the
In insects, egg clutching, in addition to improving egg predatorybehaviorofdifferentharpactorinespecies(Edwards
survival by preventing desiccation, is often associated with 1966;Inoue1982,1985;Haridassetal.1987,1988;Weirauch
toxicityorimpalatabilityandfavorslarval/nymphalaggrega- etal.2012;ZhangandWeirauch2013),weaimedtoverifyif
tion (Janz 2002) which frequently permits early instars to clutchlayingbyfemalesisfollowedbynymphclusteringwith
organize a group defense (Jolivet 2008). Feeding efficiency thesubsequentpossibilityofgrouphuntingandpreysharing
isimprovedwhenlarvalaggregationisassociatedwithcom- byexaminingthemodalitiesoftheirhuntingbehavior.
munalfeedingintheherbivorelarvaeofsawflies,chrysomelid
beetles, and lepidopterans (Wilson 1971; Grégoire 1988).
Communalfeedingisinfrequentamongpredatoryinsectsthat Materialsandmethods
lay their eggs in clutches. Group hunting and prey sharing
were noted in the first instar larvae of aphidophagous Studysiteandmodels
ladybirds(Mooreetal.2012),inthenymphsandadultsofa
predacious pentatomid (Heteroptera) (Ables 1975), and in Thisstudywasconductedbetween2009and2013atthefield
some harpactorine assassin bug nymphs (Heteroptera; stationatPetitSaut,Sinnamary,FrenchGuiana(5°03′39″N;
Reduviidae)(Inoue1982;Haridassetal.1988;Jacksonetal. 53°02′36″W)andintheforestaroundthestation;also,some
2010). Z. annulosus individuals were gathered from La Montagne
Exceptforthevertebrateblood-feedingTriatominae,other dessinges (5°04′19″N;52°41′42″W),ca.50kmawayfrom
reduviid subfamilies are almost exclusively composed of ar- Petit Saut. The climate is tropical moist, with 3,500 mm of
thropod predators (Hwang and Weirauch 2012; but see annualprecipitationdistributedover280days.
Bérenger and Plutot-Sigwalt 1997). Prey capture success in Z.annulosus wasonlyfoundonpubescentplants,mostly
most harpactorine species, related to prey size (Inoue 1985; H.physophora.Thefemaleslayeggclustersundertheleaves
Cogni et al. 2002), is enhanced by the presence of a sticky anddepositastickysecretiononthemthatseemssufficientto
substancethatcoatstheirlegs.“Resinbugs”gatherthissub- wardoffpredatorsandants.Theythenflyaway,leavingthe
stancefromcertainplants(Foreroetal.2011).Insomespecies eggs to develop unattended. Between 10 and 22 first instar
of the genus Zelus, the substance is secreted by specialized nymphshatchfromtheseeggclusters(Reveletal.2010;AD,
dermal glands and sticks to the “sundew setae” (so-called MR,andOR,personalcommunication).
because they resemble the trichomes of sundew carnivorous
plants)thatcoverthetibiaeoftheforelegs(WernerandReid ThehuntingzonesandpreysofdifferentinstarsofZ.
2001; Betz and Kölsch 2004; Weirauch 2006; Zhang and annulosus nymphs
Weirauch 2013). Because they lack these sticky glands, the
firstinstarsusethestickysecretionsdepositedbyfemaleson We surveyed 65 Hirtella trees on which we had noted the
their egg massto increasetheir predation success (Weirauch presenceofZ.annulosus nymphs,representingca.240hof
2006; Law and Sediqi 2010). Also, Agriosphorus dohrni focal samplings distributed over 80 non-consecutive days
nymphs (Harpactorinae) allocate short periods to active for- during the rainy season in which individuals were observed
agingwheretheyformsearchgroupsoftenormoreindivid- continuouslyforperiodsoftimeofmorethan2h(generally
ualsofdifferentorigins(notnecessarilysiblings);smallpreys limitedbytherainornightfall).Inaddition,duringaseriesof
are eaten selfishly, whereas large preys are shared (Inoue observations permitting us to cover the 24 h of the
1982,1985). nycthemeron, we verified each hour if the nymphs were
ThenymphsoftheassassinbugZelusannulosus areeffi- huntingorshelteringundertheleaves(35to43diurnalcon-
caciouspredatorsthatdevelopmostlyonHirtellaphysophora trols;16to48nocturnalcontrols).
(Chrysobalanaceae) (Revel et al. 2010). This is an In both approaches, we noted if, depending on the instar,
understorey-dwelling myrmecophyte (i.e., a plant housing thenymphsstayedundertheleafwheretheyhatchedorleftto
ants in hollow structures) whose long-lived leaves bear huntonitsupperside,whethertheyremainedgroupedornot,
extrafloralnectariesandapairofpouchesatthebaseofeach and finally if they moved to a different leaf. We also noted
lamina where colonies of the myrmicine ant, Allomerus whatinsectswerecapturedbythesenymphsplusinformation
ontheirsizeandtheperiodoftheyear.Usingaquartzcrystal frequenciesbetweenbehavioralacts,presentedaspercentages,
microbalance, we weighed several live preys and Z. werecalculatedbasedontheoverallnumberofcases.
annulosus nymphstocalculatetheprey–predatorweightratio
(Table1). Roleofthesundewsetaeduringthecaptureofflying
andjumpinginsects
PreycapturebehaviorbyZ.annulosus nymphs
We tested third instar nymphs bred in the same laboratory
Thisstudywasconductedonnymphsbredinthelaboratoryin conditions as previously but using larger transparent plastic
transparentplasticboxes(180×120×75mm)whosefloorwas boxes(240×180×100mm)insidewhichweinstalledapaper
covered with humid blotting paper. Each nymph, starved for shelfinonecornerofthebox,20mmbelowthecover.Two
72hafterbeingplacedintheplasticbox,wastestedonlyonce. sets of14 nymphs were starved for 72h beforeone set was
Theprotocolwasadaptedfromthatusedforsolitaryforaging providedwith27–30-mm-longadult Tipulidaeand the other
ants(seeDejean2011).Duringpreliminaryexperiments,afull with 10–12-mm-long grasshoppers. Each nymph was tested
repertoire of behavioral sequences was first established. onlyonce.Thetestedpreyswerefirstplacedinarefrigerator
Referring tothis completelist,thepreycapture behavior was at4°Cduring30minbeforebeingverygentlydepositedon
studiedinthelaboratoryusingthird(N=56)andfifth(N=28) the paper shelf in the plastic boxes so as to keep them from
instar Z. annulosus nymphs confronted with termite workers beingimmediatelydetected.Theyremainedimmobileduring
(Nasutitermes nigriceps) which are easy to find and rather 5–6 min before leaving the paper shelf and were captured
uniforminsize.Afterapreywasdroppedfromca.50mmin whentheyhappenedtowalkclosetotheambushingnymphs.
height,werecordedthecompletesequenceofbehavioralacts Wenotedthebehavioralsequences.
performedbythenymphsuntiltheyabandonedtheremainsof
the prey. We then built flow diagrams where the transition PreysharingbyZ.annulosus nymphs:influenceofpreysize,
predatorsize,anddegreeofhunger
Table1 Informationonthepredator–preyweightratioforthedifferent
cases studied. The weight of the Zelus annulosus nymphs and adults We verified iffirst instar nymphs, although fragile in appear-
correspondstoanaverageforfivetotenindividualsstarvedfor4days
ance, are able to capture and share preys. Using smooth for-
Size(mm) Weight(mg) ceps, we gathered nine groups of nymphs and placed each
groupinatransparentplasticboxandtransportedthemtothe
Z.annulosus laboratory.Afterstarvingthemfor24handstillusingsmooth
Firstinstarnymphs 4 2.8 forceps,wedepositedthemontheuppersideofahorizontalH.
Secondinstarnymphs 5–6 6.0 physophora leafplaced in the plastic boxes. After 5 min, the
Thirdinstarnymphs 8–10 17.0 nymphs apparently adapted to this situation as they did not
Fourthinstarnymphs 12–14 35.5 immediatelymoveundertheleavesandremainedgrouped.We
Fifthinstarnymphs 18–20 63.0 droppedatermitefromca.50mminheightontothecenterof
Adults 21–24 67.5 theleafandnotedifthenymphscapturedandsharedtheprey.
RatiobetweentheweightofexperimentalpreyandZ.annulosusnymphs Wetestedtheinfluenceofthedegreeofstarvationandthe
Nasutitermesnigricepsworkers 4–5mm 9–12mg sizeofthepreysinaseriesofexperimentsbasedongroupsof
Firstinstarnymphs 3.21to4.28 fiveorsixsecondinstarnymphs.Webredthemintransparent
Secondinstarnymphs 1.50to2.00 plastic boxes (240×180×100 mm) where we placed an old,
Thirdinstarnymphs 0.53to0.71 resistant Hirtella leaf (they have an acumen; see Grangier
Fifthinstarnymphs 0.14to0.19 etal. 2008a) maintained30mmabove the floor, thanks toa
Tipulidae 27–30mm 17–25mg piece of modeling clay. Also, a small test tube containing
Thirdinstarnymphs 1to1.47 cotton imbibed with water served as a watering place. After
Grasshoppers 10–12mm 35–44mg being starved for 96 h, 14 groups of nymphs were provided
Thirdinstarnymphs 2.06to2.59 withonetermiteworker;weverifiedifthenymphssharedthe
Katydids 12–14mm 80–100mg prey.Afterthesameperiodofstarvation,14othergroupsof
Secondinstarnymphs 13.33to16.67 nymphs were provided with 12–14-mm-long katydids and
here,too,weverifiedifthepreyswereshared;36hlater,we
Fourthinstarnymphs 2.53to2.82
providedthese14groups(theywerenotyetfooddeprivedas
Fifthinstarnymphs 1.27to1.59
Katydids 19–20mm 135–150mg they had eaten a katydid 36 h before) with a termite worker
andagainnotedifthepreysweresharedornot.
Secondinstarnymphs 22.50to25.00
Furtherobservationsweremadeintheforesttoverifyifthe
Thirdinstarnymphs 7.94to8.82
behaviorsdifferedfromthosenotedinthelaboratory.Wealso
testedifsecondinstarnymphsgatheredfromplantsoriginat- exceptionally climbed up onto the upper side of that leaf
ing from different geographic areas (i.e., Petit Saut and La where they all sat and waited, their forelegs upward,
Montagne des singes) tolerate each other by creating eight ambushinginagroup(notedonceforeightgroupsmonitored
mixedgroups(threeindividualsfromeachsite)thatwerebred hourly between 8:00 and 18:00 hours during six non-
intransparent plastic boxes (180×120×75mm) whose floor consecutivedays).Thesecondandthirdinstarnymphsdevot-
was covered with humid blotting paper. We furnished them edmuchmoretimetogroupambushingontheuppersideof
with 19–20-mm-long katydids as prey and verified if the their leaves (noted 28 times for the eight groups monitored
nymphsremainedgrouped,ifthereweresignsofaggressive- during12non-consecutivedays,thetwoinstarspooled;com-
ness,andiftheysharedthesepreys. parisonwiththepreviouscase,Fisher’sexacttest:P<0.001).
Therestofthedayandatnight,nymphsofallstagesremain
ArenymphsattractedwhenpreysaresharedbylateinstarZ. groupedundertheprotectionoftheirleaves;huntingnymphs
annulosus nymphs? immediately sheltered under the leaves when the rain began
(27casesnoted).Weobservedthatlessthan5minseparated
Late instar nymphs fan out over different Hirtella leaves to themomentwhenthefirstandthelastindividualclimbedup
ambush (MR, personal communication). Because we noted ontotheuppersideoftheirleaftoambushinagroup.Onthe
that they shared preys, we hypothesized that a successful contrary,diurnally,thefourthandfifthinstarnymphsmostly
nymph can attract tree-mates. Due to the horizontal position ambushed solitarily on different leaves as they are large
ofHirtella leaves,itwaseasytoeliminatethevisualcuesthat enough to avoid the traps built by Allomerus ants as they
canattractindividualsambushingonlowerleavesbyplacing slowly move from leaf to leaf. This was the case for 47
apreyononeoftheupperleaves.Weverygentlyplaceda12– observations out of 96 (12 series of observations of eight
14-mm-longnumbed(byfreezing)katydidontheuppermost groups,thetwoinstarspooled;48.9%),buttwicetheywere
leafofeachsurveyedHirtella treewhilefourthorfifthinstar groupedonaleaf(2.1%;butseebelow).
nymphswereambushingonlowerleavesandnotedthenum- Because theyambushonthe leavesoftheir hosttrees,Z.
berofnymphspresentonthatleafafter30minoffeedingon annulosus nymphs captured flying insects almost uniquely,
the katydid. We compared two situations (25 cases each): the exceptions being jumping Orthoptera nymphs (Table 2).
absence (control) versus presence (trial) of an ambushing Thesecondinstarnymphscapturedonlysmall(i.e.,lessthan
nymphontheupperleafwhenwedepositedthekatydid. 8mm),fragilepreys(i.e.,AleyrodidaeanddifferentDiptera;
In22casessimilartothepreviouscontrol(herecontrol1),we likely underrepresented in Table 2), while larger instars
notedthelengthoftimeseparatingthedepositingofthekatydid attacked almost all insects that tried to land on their leaf,
fromthearrivalofafirstnymph.For11ofthesecases,wewaited includingitemslargerthanthemselves.Seasonalitywasnoted
untilasecondnympharrived(trial1);forthe11othercases,we for certain preys as all horse flies were captured in October
removedthefirstnymphpriortoitattackingthekatydid(control (when they abound during the dry season), winged termites
2). In both cases, we noted the length of time separating the were captured after the first rains in December and January
arrival of the first and second nymphs. These data were com- andwingedantsbetweenmid-DecemberandMarch.
paredwith15caseswhereanymphwasambushingontheupper TheZ.annulosus nymphscanfeedonthepreycapturedby
leaf, noting the length of time separating the depositing of the theAllomerus ontheirtrap(cleptobiosiswasnotedninetimes)
katydidfromthearrivalofa“second”nymph(trial2). or on flies, social wasps, and stingless bees attracted by these
In a third experiment, conducted on 16 Hirtella trees capturedpreys.
sheltering last instar Zelus nymphs, we deposited two katy-
didsontwo lower leaveswhile a nymph was ambushing on PreycapturebehaviorbyZ.annulosus nymphs(laboratory
oneofthem.We comparedthe lengthoftimeseparatingthe studies)
depositingofthekatydidsfromthearrivalofanymphoneach
of the two leaves. Statistical analyses were conducted using The predatory sequences developed by small and large Z.
GraphPadPrism5.02software. annulosus nymphswerequitesimilaralthoughthepredator–
prey weight ratios were different (see Table 1). When
ambushing, nymphs generally lift and spread their forelegs.
Results Preys,detectedfromadistancebyvisualorchemicalcuesor
vibrations, were cautiously approached; the nymphs lifting
ThehuntingzonesandpreysofdifferentinstarsofZ. their forelegs higher than previously. When at an adequate
annulosus nymphs distance,theyslammedtheirforelegsdownonthepreysstuck
onthesundewsetae;then,thenymphsextendedtheirrostrum
In the field, the first instar nymphs remained grouped under toward the preys to bite them in an inter-segmental zone,
the leaf where they hatched until the first molt and only paralyzing them. The Z. annulosus lifted the preys by
Table2 Differentarthropodtaxa
capturedundernaturalconditions Insectprey Size No.ofcases Insectprey Size No.ofcases
byZelusannulosus(N=308) (mm) (mm)
Ephemeroptera(mayflies) 24 1 Thysanoptera,Thripidae 6–7 11
Odonata,Lestidae(damselflies) 23 1 Neuroptera,Chrysopidae 12–14 2
Orthoptera – – Coleoptera – –
Tettigoniidae(katydids) 11–15 15 Chrysomelidae 6–15 23
– >25 6 Lampyridae(fireflies) 11–13 3
Gryllidae(crickets) 11–15 8 Cerambycidae 21 1
– >25 2 Diptera – –
Acrididae(grasshoppers) 11–15 12 CulicidaeandCecidomyiidae 7 6
– >25 4 TachinidaeandCalliphoridae <10 24
Mantodea(prayingmantises) 24 1 (Flies) >10 4
Blattaria(cockroaches) – – Tabanidae(horseflies) 11 14
– <25 17 Tipulidae(craneflies) 15–18 17
– 25–40 8 – 30–35 11
Isoptera(termites) – – Drosophilidae(fruitflies) <5 20
Wingedtermites 10–15 12 Otherflies 4–6 13
Dermaptera(earwings) 14 1 Lepidoptera
Psocoptera 5 2 Rhopalocera(butterflies) 20–22 7
Hemiptera – – Heterocera(moths) 11–25 6
Aleyrodidae 6–7 4 Hymenoptera – –
Cicadellidae 7–8 2 Ichneumonidae 24–28 2
Membracidae 8–10 2 Vespidae,Polistinae – –
aAttractedbyapreyalreadyin Fulgoromorpha 8–12 2 Angiopolybiapallensa 11 7
theprocessofbeingeatenby Sap-suckingHeteroptera 12–18 7 Formicidae(winged) 7–16 17
Zelusannulosusnymphsand Reduviidae(assassinbugs)a 20–22 4 Apidae;Trigonaa 11 9
capturedinturn
extendingtheirrostrumandlaterusedtheirforelegstorotate remaining grasshoppers, three were mastered on the first
the preys while injecting saliva and sucking out digested attemptalthoughtheydidnotlosetheirhindlegsandthelast
matter; the corresponding parts of the preys turned black. oneescaped.Here,too,thebitetriggeredimmediateparalysis.
TheZ.annulosus nymphscanrepeatedlyrotateandbitethe Aswasnotedfortermites,afterbecomingparalyzed,boththe
preysuptotentimesbeforediscardingtheemptiedoutpreys Tipulidaeandthekatydidswererotatedandbittennumerous
(Figs.1and2). timesbeforebeingabandoned.
Roleofthesundewsetaeduringthecaptureofflying PreysharingbyZ.annulosus nymphs:influenceofpreysize,
andjumpinginsects(laboratorystudies) predatorsize,anddegreeofhunger(laboratorystudies)
Both tested preys were detected by sight immediately after Alltestedgroupsofstarvedfirstinstarnymphsalmostsimul-
they began to leave the paper shelf on which they had been taneouslyattackedandthensharedatermiteprey.
deposited; indeed, the nymphs oriented their bodies in the Althoughthesizebetweentermiteworkersandkatydidsis
preys’ direction while lifting their antennae and forelegs. not the only difference, the importance of prey size likely
The attacks occurred immediately after the preys happened explainsthedifferencenotedwhenstarvedgroupsofsecond
to approach the nymphs to less than 20 mm. All of the 14 instarnymphssharedatermiteworkerinonly28.6%ofthe
testedTipulidaewerecapturedinflightonthefirstattemptas cases, while they shared a much larger katydid in all cases.
one or both of their long, thin wings became stuck to the Theeffectofhungerwasillustratedas36haftercapturinga
nymphs’ forelegs and they became paralyzed after being katydidaspreythese“ratherreplete”nymphsthistimeshared
bitten.Among the 14testedgrasshoppers,10(71.4%)were atermiteworkerin92.8%ofthecases(Fig.3;seealsoprey
masteredonthefirstattemptbecausetheylosttheirhindlegs sharinginnaturalconditionsinFig.2).
through autotomy at contact with the sundew setae of the When the captured termites were not shared, the nymph
Zelus nymphs’ forelegs (see Fig. 2d). Among the four thatsuccessfullycapturedthemmovedawayfromitssiblings.
Fig.1 FlowdiagramsrepresentingthesequencesofthehuntingbehaviorofZ.annulosus nymphsoftwosizeclassesduringthecaptureoftermite
workers.Thepercentageswerecalculatedfromthetotalnumberofcases
Fig.2 Captureofgrasshoppers
andkatydidsbyZ.annulosus.a
Asmallgrasshopperwasjust
seizedandbittenbyafifthinstar
nymph.b Agrasshopperis
rotatedandbitteninseveralparts.
cAkatydidnymphwasjust
capturedbyafifthinstarnymph
andhadlostonehindleginthe
process.d Asmallgrasshopper,
capturedbyanadultZelus,had
lostitshindlegsthrough
autotomy;thelatterarestillglued
totheforelegsoftheZelus.The
horizontalbarsrepresent10mm.
eTwonymphssharingafly.fAn
adultkatydidwascapturedbya
fifthinstarnymphandisnow
beingsharedwiththreeother
nymphs,oneofthembitingthis
preyonthejointbetweenthe
femurandthetibiaofthehindleg
Attheendofthesequence,itwalkedtothetipoftheHirtella from all eight artificial groups remained grouped exactly as
leaf,placeditsheadabovetheextremityofthenarrowacumen, didsiblingsandthattheysimilarlysharedthetestedpreys.
andselfishlyatethetermite.Indeed,noneoftheothernymphs
triedtoreachthepreyfromtheundersideoftheleaf,anditwas ArenymphsattractedwhenpreysaresharedbylateinstarZ.
outoftheirreachfromtheupperside.Thesamewasnotedfor annulosus nymphs?
fivecasesduringcontrolsconductedintheforest.
WhentestingifZ.annulosus nymphsfromdifferentgeo- Fromfieldstudies,wehavegatheredargumentsshowingthat
graphicareascanformmixedgroups,wenotedthatnymphs Z. annulosus nymphs successful at capturing a prey likely
Fig.3 Preysharingaccordingto
itssizeandthedegreeofhunger
ofsecondinstarZ.annulosus
nymphs(N=14ineachcase).
Statisticalcomparison:Fisher’s
exacttests;simultaneoustests
wereadjustedusingthefalse
discoveryrate(“BY”correction
astheP valuesarenot
independent;Pike2011);different
lettersindicatesignificant
differencesatP<0.01
attract siblings; the tests being based on comparing nymphs ants,weshowthatZ.annulosusfirstinstarnymphsareableto
attractedtowardapreyalone(controls)totheirattractiontoa capture and share comparatively large preys of up to 4.28
preyalreadyhavingbeencapturedbyasibling(trials).First, timestheirweight(Table1).Thiscapacitylikelypermitsthem
30 min after a nymph had begun to feed on the numbed toavoidlethalstarvationwhichisrecurrentintropicalspecies
katydid provided, we noted significantly more nymphs on (MaranandAmbrose2000).Innaturalconditions,fewflying
these leaves (trial) than on control leaves (2.64±0.21 vs. insectsofadequatesizearepronetoalightundertheleavesof
0.36±0.11; N=25 ineach case; Welch’s corrected t test: t= their host plant so that their main preys are adults of gall-
9.371;df=36;P<0.0001).Second,wedidnotnoteasignif- making Cecidomyiidae, which are frequent under the leaves
icantdifferencebetweencontrol1(lengthoftimeseparating ofshrubsintheunderstorey(AD,personalobservation).
our depositing a numbed katydid and the arrival of a first The sequences of behavioral acts during prey capture by
nymph)andcontrol2(whenweremovedthefirstnymphthat solitary nymphs were very similar to those known for other
reachedtheleafwherewehaddepositedthekatydid)(Fig.4). Harpactorinae, except that Z. annulosus ambush preys and
The length of time corresponding to these controls was sig- detectthemfroma“long”distance,while,inotherspecies,the
nificantlylongerthanthatcorrespondingtotrial1(i.e.,sepa- nymphs forage actively and frequently detect the preys
ratingthearrivalofthetwofirstnymphs)andtrial2(i.e.,an through antennalcontact (Edwards1966; Inoue 1982, 1985;
ambushingnymphwasalreadypresent),whilethedifference Haridassetal.1987,1988;Jacksonetal.2010;Weirauchetal.
between these latter situations was not significant (Fig. 4). 2012).Sundewsetae are known toplayanimportantrolein
Third,thelengthoftimeseparatingthedepositingofkatydids thecaptureofcaterpillarsandsmallflyinginsects(Weirauch
onto two lower leaves of 16 Hirtella trees to the arrival of a etal. 2012; Zhang and Weirauch 2013).Here, we showthat
“new”lastinstarnymphwassignificantlyshorterwhenaZelus theypermitthecaptureoflargeinsectspronetoescapeeasily
nymphwaspresent(trials)thanforthecontrols(25.5±1.9vs. by flying or jumping away. Furthermore, contact with the
14.3±0.9min;pairedt test:t=5.47;df=15;P<0.0001). sundew setae of the Zelus nymphs’ forelegs triggered the
autotomy of the hind legs of a grasshopper in 10 out of 14
cases. Autotomy, a mechanism designed to help an insect
Discussion eludea predator’s grasp,occurredhereatthe expense ofthe
prey.Finally,inallcases,theinjectionofsalivawasdetermi-
Although they are apparently fragile and never leave the nant due to its fast, non-lethal paralytic effect related to the
underside of the H. physophora leaves where they hatched presenceofneurotoxiccompounds(seeMaranandAmbrose
(Reveletal.2010)sincetheyriskbeingtrappedbyAllomerus 2000;Corzoetal.2001;SahayarajandVinothkanna2011).
Fig.4 Comparisonofthelengthoftime(means±SE)between(1)our (4) between our depositing of a numbed katydid on the uppermost
depositing of a numbed katydid on the uppermost horizontal leaf of horizontalleafonwhichanymphwasalreadyambushingandthearrival
Hirtella treesandthearrivalofthefirstZ.annulosus nymph(control1 ofasecondnymph(experiment2).Statisticalcomparison;ANOVA:F=
inthetext),(2)thearrivalofthesecondnymph(experiment1),(3)the 19.77;P<0.001;Newman–Keulsposthoctest:differentlettersindicatea
arrivalofthesecondnymph,whereaswehadremovedthefirstnymph significantdifferenceatP<0.001
thatreachedtheleafwherewehaddepositedthekatydid(control2),and