Appetite for self-destruction: suicidal biting as a nest defense strategy in Trigona stingless bees
Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness benefits are high, such as when defending the nest. We studied nest defense behaviors in stingless bees, which live in eusocial colonies subject t...
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Published in | Behavioral ecology and sociobiology Vol. 69; no. 2; pp. 273 - 281 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
Berlin/Heidelberg
Springer
01.02.2015
Springer Berlin Heidelberg Springer Nature B.V |
Subjects | |
Online Access | Get full text |
ISSN | 0340-5443 1432-0762 |
DOI | 10.1007/s00265-014-1840-6 |
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Abstract | Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness benefits are high, such as when defending the nest. We studied nest defense behaviors in stingless bees, which live in eusocial colonies subject to predation. We introduced a target flag to nest entrances to elicit defensive responses and quantified four measures of defensivity in 12 stingless bee species in Sao Paulo State, Brazil. These included three Trigona species, which are locally known for their aggression. Species varied significantly in their attack probability (cross species range=0-1, P<0.001), attack latency (7.0-23.5 s, P=0.002), biting duration of individual bees (3.5-508.7 s, P<0.001), and number of attackers (1.0-10.8, P<0.001). A "suicide" bioassay on the six most aggressive species determined the proportion of workers willing to suffer fatal damage rather than disengage from an intruder. All six species had at least some suicidal individuals (7-83 %, P<0.001), reaching 83 % in Trigona hyalinata. Biting pain was positively correlated with an index of overall aggression (P=0.002). Microscopic examination revealed that all three Trigona species had five sharp teeth per mandible, a possible defensive adaptation and cause of increased pain. Suicidal defense via biting is a new example of selfsacrificial altruism and has both parallels and differences with other self-sacrificial worker insects, such as the honey bee. Our results indicate that suicidal biting may be a widespread defense strategy in stingless bees, but it is not universal. |
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AbstractList | Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness benefits are high, such as when defending the nest. We studied nest defense behaviors in stingless bees, which live in eusocial colonies subject to predation. We introduced a target flag to nest entrances to elicit defensive responses and quantified four measures of defensivity in 12 stingless bee species in Sao Paulo State, Brazil. These included three Trigona species, which are locally known for their aggression. Species varied significantly in their attack probability (cross species range=0-1, P<0.001), attack latency (7.0-23.5 s, P=0.002), biting duration of individual bees (3.5-508.7 s, P<0.001), and number of attackers (1.0-10.8, P<0.001). A "suicide" bioassay on the six most aggressive species determined the proportion of workers willing to suffer fatal damage rather than disengage from an intruder. All six species had at least some suicidal individuals (7-83 %, P<0.001), reaching 83 % in Trigona hyalinata. Biting pain was positively correlated with an index of overall aggression (P=0.002). Microscopic examination revealed that all three Trigona species had five sharp teeth per mandible, a possible defensive adaptation and cause of increased pain. Suicidal defense via biting is a new example of self-sacrificial altruism and has both parallels and differences with other self-sacrificial worker insects, such as the honey bee. Our results indicate that suicidal biting may be a widespread defense strategy in stingless bees, but it is not universal. Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness benefits are high, such as when defending the nest. We studied nest defense behaviors in stingless bees, which live in eusocial colonies subject to predation. We introduced a target flag to nest entrances to elicit defensive responses and quantified four measures of defensivity in 12 stingless bee species in São Paulo State, Brazil. These included three Trigona species, which are locally known for their aggression. Species varied significantly in their attack probability (cross species range = 0-1, P < 0.001), attack latency (7.0-23.5 s, P = 0.002), biting duration of individual bees (3.5-508.7 s, P < 0.001), and number of attackers (1.0-10.8, P < 0.001). A "suicide" bioassay on the six most aggressive species determined the proportion of workers willing to suffer fatal damage rather than disengage from an intruder. All six species had at least some suicidal individuals (7-83 %, P < 0.001), reaching 83 % in Trigona hyalinata. Biting pain was positively correlated with an index of overall aggression (P = 0.002). Microscopic examination revealed that all three Trigona species had five sharp teeth per mandible, a possible defensive adaptation and cause of increased pain. Suicidal defense via biting is a new example of self-sacrificial altruism and has both parallels and differences with other self-sacrificial worker insects, such as the honey bee. Our results indicate that suicidal biting may be a widespread defense strategy in stingless bees, but it is not universal.Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness benefits are high, such as when defending the nest. We studied nest defense behaviors in stingless bees, which live in eusocial colonies subject to predation. We introduced a target flag to nest entrances to elicit defensive responses and quantified four measures of defensivity in 12 stingless bee species in São Paulo State, Brazil. These included three Trigona species, which are locally known for their aggression. Species varied significantly in their attack probability (cross species range = 0-1, P < 0.001), attack latency (7.0-23.5 s, P = 0.002), biting duration of individual bees (3.5-508.7 s, P < 0.001), and number of attackers (1.0-10.8, P < 0.001). A "suicide" bioassay on the six most aggressive species determined the proportion of workers willing to suffer fatal damage rather than disengage from an intruder. All six species had at least some suicidal individuals (7-83 %, P < 0.001), reaching 83 % in Trigona hyalinata. Biting pain was positively correlated with an index of overall aggression (P = 0.002). Microscopic examination revealed that all three Trigona species had five sharp teeth per mandible, a possible defensive adaptation and cause of increased pain. Suicidal defense via biting is a new example of self-sacrificial altruism and has both parallels and differences with other self-sacrificial worker insects, such as the honey bee. Our results indicate that suicidal biting may be a widespread defense strategy in stingless bees, but it is not universal. Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness benefits are high, such as when defending the nest. We studied nest defense behaviors in stingless bees, which live in eusocial colonies subject to predation. We introduced a target flag to nest entrances to elicit defensive responses and quantified four measures of defensivity in 12 stingless bee species in Sao Paulo State, Brazil. These included three Trigona species, which are locally known for their aggression. Species varied significantly in their attack probability (cross species range=0-1, P<0.001), attack latency (7.0-23.5 s, P=0.002), biting duration of individual bees (3.5-508.7 s, P<0.001), and number of attackers (1.0-10.8, P<0.001). A "suicide" bioassay on the six most aggressive species determined the proportion of workers willing to suffer fatal damage rather than disengage from an intruder. All six species had at least some suicidal individuals (7-83 %, P<0.001), reaching 83 % in Trigona hyalinata. Biting pain was positively correlated with an index of overall aggression (P=0.002). Microscopic examination revealed that all three Trigona species had five sharp teeth per mandible, a possible defensive adaptation and cause of increased pain. Suicidal defense via biting is a new example of selfsacrificial altruism and has both parallels and differences with other self-sacrificial worker insects, such as the honey bee. Our results indicate that suicidal biting may be a widespread defense strategy in stingless bees, but it is not universal. Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness benefits are high, such as when defending the nest. We studied nest defense behaviors in stingless bees, which live in eusocial colonies subject to predation. We introduced a target flag to nest entrances to elicit defensive responses and quantified four measures of defensivity in 12 stingless bee species in São Paulo State, Brazil. These included three Trigona species, which are locally known for their aggression. Species varied significantly in their attack probability (cross species range = 0–1, P < 0.001), attack latency (7.0–23.5 s, P = 0.002), biting duration of individual bees (3.5–508.7 s, P < 0.001), and number of attackers (1.0–10.8, P < 0.001). A “suicide” bioassay on the six most aggressive species determined the proportion of workers willing to suffer fatal damage rather than disengage from an intruder. All six species had at least some suicidal individuals (7–83 %, P < 0.001), reaching 83 % in Trigona hyalinata . Biting pain was positively correlated with an index of overall aggression ( P = 0.002). Microscopic examination revealed that all three Trigona species had five sharp teeth per mandible, a possible defensive adaptation and cause of increased pain. Suicidal defense via biting is a new example of self-sacrificial altruism and has both parallels and differences with other self-sacrificial worker insects, such as the honey bee. Our results indicate that suicidal biting may be a widespread defense strategy in stingless bees, but it is not universal. Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness benefits are high, such as when defending the nest. We studied nest defense behaviors in stingless bees, which live in eusocial colonies subject to predation. We introduced a target flag to nest entrances to elicit defensive responses and quantified four measures of defensivity in 12 stingless bee species in São Paulo State, Brazil. These included three Trigona species, which are locally known for their aggression. Species varied significantly in their attack probability (cross species range = 0–1, P < 0.001), attack latency (7.0–23.5 s, P = 0.002), biting duration of individual bees (3.5–508.7 s, P < 0.001), and number of attackers (1.0–10.8, P < 0.001). A “suicide” bioassay on the six most aggressive species determined the proportion of workers willing to suffer fatal damage rather than disengage from an intruder. All six species had at least some suicidal individuals (7–83 %, P < 0.001), reaching 83 % in Trigona hyalinata. Biting pain was positively correlated with an index of overall aggression (P = 0.002). Microscopic examination revealed that all three Trigona species had five sharp teeth per mandible, a possible defensive adaptation and cause of increased pain. Suicidal defense via biting is a new example of self-sacrificial altruism and has both parallels and differences with other self-sacrificial worker insects, such as the honey bee. Our results indicate that suicidal biting may be a widespread defense strategy in stingless bees, but it is not universal. Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness benefits are high, such as when defending the nest. We studied nest defense behaviors in stingless bees, which live in eusocial colonies subject to predation. We introduced a target flag to nest entrances to elicit defensive responses and quantified four measures of defensivity in 12 stingless bee species in São Paulo State, Brazil. These included three species, which are locally known for their aggression. Species varied significantly in their attack probability (cross species range = 0-1, < 0.001), attack latency (7.0-23.5 s, = 0.002), biting duration of individual bees (3.5-508.7 s, < 0.001), and number of attackers (1.0-10.8, < 0.001). A "suicide" bioassay on the six most aggressive species determined the proportion of workers willing to suffer fatal damage rather than disengage from an intruder. All six species had at least some suicidal individuals (7-83 %, < 0.001), reaching 83 % in . Biting pain was positively correlated with an index of overall aggression ( = 0.002). Microscopic examination revealed that all three species had five sharp teeth per mandible, a possible defensive adaptation and cause of increased pain. Suicidal defense via biting is a new example of self-sacrificial altruism and has both parallels and differences with other self-sacrificial worker insects, such as the honey bee. Our results indicate that suicidal biting may be a widespread defense strategy in stingless bees, but it is not universal. |
Author | Alves, Denise A. Nascimento, Fabio S. Ratnieks, Francis L. W. Toufailia, Hasan Al Balfour, Nicholas J. Shackleton, Kyle |
Author_xml | – sequence: 1 givenname: Kyle surname: Shackleton fullname: Shackleton, Kyle – sequence: 2 givenname: Hasan Al surname: Toufailia fullname: Toufailia, Hasan Al – sequence: 3 givenname: Nicholas J. surname: Balfour fullname: Balfour, Nicholas J. – sequence: 4 givenname: Fabio S. surname: Nascimento fullname: Nascimento, Fabio S. – sequence: 5 givenname: Denise A. surname: Alves fullname: Alves, Denise A. – sequence: 6 givenname: Francis L. W. surname: Ratnieks fullname: Ratnieks, Francis L. W. |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25620834$$D View this record in MEDLINE/PubMed |
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Keywords | Nest guards Stingless bees Colony defense Self-destructive behavior Self-sacrifice Trigona |
Language | English |
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References | BrownRMDahlenEMillsCRickJBiblarzAEvaluation of an evolutionary model of self-preservation and self-destructionSuicide Life Threat19992958711:STN:280:DyaK1M3lsF2gsw%3D%3D Bates D, Maechler M, Bolker B, Walker S (2013) lme4: linear mixed-effects models using Eigen and S4. R package version. Vol. 1 R Core TeamR: a language and environment for statistical computing2014ViennaR Foundation for Statistical ComputingURL http://www.R-project.org SchmidtJOEvansDLSchmidtJOHymenopteran venoms: striving towards the ultimate defense against vertebratesInsect defenses: adaptive mechanisms of prey and predators1990AlbanyState University of New York Press387420 AlockJAnimal behaviour20058MassachusettsSinauer Associates, Inc. SukaTInoueTNestmate recognition of the stingless bee Trigona (Tetragonula) minangkabau (Apidae: Meliponinae)J Ethol19931114114710.1007/BF02350047 Pinheiro J, Bates D, DebRoy S, Sarkar D and R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1-117 SommeijerMJDistribution of labour among workers of Melipona favosa F.: age-polyethism and worker ovipositionInsect Soc19843117118410.1007/BF02232713 HuntGJGuzmán-NovoaEFondrkMKPageREQuantitative trait loci for honey bee stinging behavior and body sizeGenetics1998148120312131:CAS:528:DyaK1cXks1eit7c%3D14600549539435 SeeleyTDHoneybee ecology: a study of adaptation in social life1985New JerseyPrinceton University Press Shackleton K, Al Toufailia H, Balfour N, Alves D, Nascimento F, Ratnieks Shackleton K, Al Toufailia H, Balfour N, Alves D, Nascimento F, Ratnieks R (2014) Appetite for self-destruction: suicidal biting as a nest defense strategy in Trigona stingless bees. ZENODO. doi:10.5281/zenodo.12522 NagamitsuTInoueTAggressive foraging of social bees as a mechanism of floral resource partitioning in an Asian tropical rainforestOecologia199711043243910.1007/s004420050178 GrüterCMenezesCImperatriz-FonsecaVRatnieksFLA morphologically specialized soldier caste improves colony defense in a neotropical eusocial beeProc Natl Acad Sci U S A20121091182118632683332223268810.1073/pnas.1113398109 de CatanzaroDA mathematical model of evolutionary pressures regulating self-preservation and self-destructionSuicide Life Threat198616166181 WilleABiology of the stingless beesAnnu Rev Entomol198328416410.1146/annurev.en.28.010183.000353 OnoMIgarashiTOhnoESasakiMUnusual thermal defence by a honeybee against mass attack by hornetsNature199530733433610.1038/377334a0 MichenerCDThe bees of the world2000BaltimoreJohns Hopkins University Press MaschwitzUMaschwitzEPlatzende arbeiterinnen: eine neue art der feindabwehr bei sozialen HautflüglernOecologia19741428929410.1007/BF01039798 HermannHRSting autotomy, a defensive mechanism in certain social HymenopteraInsect Soc19711811112010.1007/BF02223116 RoubikDWObligate necrophagy in a stingless beeScience1982217105910601:STN:280:DC%2BC3cvlvFGitw%3D%3D1783934310.1126/science.217.4564.1059 UematsuKKutsukakeMFukatsuTShimadaMShibaoHAltruistic colony defense by menopausal female insectsCurr Biol201020118211861:CAS:528:DC%2BC3cXoslajtrw%3D2061981710.1016/j.cub.2010.04.057 ShorterJRRueppellOA review on self-destructive defense behaviors in social insectsInsect Soc20125911010.1007/s00040-011-0210-x BuchwaldRBreedMDNestmate recognition cues in a stingless bee, Trigona fulviventrisAnim Behav2005701331133710.1016/j.anbehav.2005.03.017 NonacsPAlloparental care and eusocial evolution: the limits of Queller's head-start advantageOikos19912912212510.2307/3545413 SefcKMMattersdorferKSturmbauerCKoblmüllerSHigh frequency of multiple paternity in broods of a socially monogamous cichlid fish with biparental nest defenceMol Ecol200817253125431:CAS:528:DC%2BD1cXotVOksLw%3D1843014610.1111/j.1365-294X.2008.03763.x Burrell BD, Smith BH (1995) Modulation of the honey bee (Apis mellifera) sting response by octopamine. J Insect Physiol 41:671–680 RoubikDWStingless bee nesting biologyApidologie20063712414310.1051/apido:2006026 TofilskiAInfluence of age polyethism on longevity of workers in social insectsBehav Ecol Sociobiol20025123423710.1007/s00265-001-0429-z MichenerCDReproductive efficiency in relation to colony size in hymenopterous societiesInsect Soc19641131734210.1007/BF02227433 PrestwichGDChemical defense by termite soldiersJ Chem Ecol197954594801:CAS:528:DyaE1MXlt1Sls74%3D10.1007/BF00987930 BordereauCRobertATuyenVVPeppuyASuicidal defensive behaviour by frontal gland dehiscence in Globitermes sulphureus Haviland soldiers (Isoptera)Insect Soc19974428929710.1007/s000400050049 van ZwedenJSGrüterCJonesSMRatnieksFLWHovering guards of the stingless bee Tetragonisca angustula increase colony defensive perimeter as shown by intra and inter-specific comparisonsBehav Ecol Sociobiol2011651277128210.1007/s00265-011-1141-2 TofilskiACouvillonMJEvisonSEFHelanteräHRobinsonEJHRatnieksFLWPreemptive defensive self‐sacrifice by ant workersAm Nat2008172E239E24310.1086/591688 NazarethTMMachadoGMating system and exclusive postzygotic paternal care in a Neotropical harvestman (Arachnida: Opiliones)Anim Behav20107954755410.1016/j.anbehav.2009.11.026 SchmidtJOBlumMSOveralWLHemolytic activities of stinging insect venomsArch Insect Biochem1983115516010.1002/arch.940010205 CouvillonMJRobinsonEJHAtkinsonBChildLDentKRRatnieksFLWEn garde: rapid shifts in honeybee, Apis mellifera, guarding behaviour are triggered by onslaught of conspecific intrudersAnim Behav2008761653165810.1016/j.anbehav.2008.08.002 KlempererHGParental behaviour in Copris lunaris (Coleoptera, Scarabaeidae): care and defence of brood balls and nestEcol Entomol1982715516710.1111/j.1365-2311.1982.tb00654.x AnderssonMWiklundCGRundgrenHParental defence of offspring: a model and an exampleAnim Behav19802853654210.1016/S0003-3472(80)80062-5 CouvillonMJWenseleersTImperatriz-FonsecaVLNogueira-NetoPRatnieksFLWComparative study in stingless bees (Meliponini) demonstrates that nest entrance size predicts traffic and defensivityJ Evol Biol2008211942011:STN:280:DC%2BD1c%2FgsFartA%3D%3D18021200 JohnsonLKHubbellSPAggression and competition among stingless bees: field studiesEcology19745512012710.2307/1934624 KerrWEde LelloESting glands in stingless bees: a vestigial character (Hymenoptera: Apidae)J New York Entomol Soc196270190214 DavidsonDWSalimKABillenJHistology of structures used in territorial combat by Borneo’s “exploding ants”Acta Zool20129348749110.1111/j.1463-6395.2011.00523.x J Alock (1840_CR1) 2005 R Core Team (1840_CR27) 2014 MJ Sommeijer (1840_CR36) 1984; 31 HR Hermann (1840_CR13) 1971; 18 GJ Hunt (1840_CR14) 1998; 148 P Nonacs (1840_CR23) 1991; 29 JO Schmidt (1840_CR30) 1990 M Andersson (1840_CR2) 1980; 28 1840_CR3 LK Johnson (1840_CR15) 1974; 55 CD Michener (1840_CR19) 1964; 11 D Catanzaro de (1840_CR11) 1986; 16 1840_CR34 1840_CR7 TD Seeley (1840_CR32) 1985 CD Michener (1840_CR20) 2000 KM Sefc (1840_CR33) 2008; 17 DW Roubik (1840_CR28) 1982; 217 R Buchwald (1840_CR6) 2005; 70 A Tofilski (1840_CR38) 2002; 51 MJ Couvillon (1840_CR9) 2008; 76 T Nagamitsu (1840_CR21) 1997; 110 MJ Couvillon (1840_CR8) 2008; 21 T Suka (1840_CR37) 1993; 11 DW Davidson (1840_CR10) 2012; 93 RM Brown (1840_CR5) 1999; 29 A Wille (1840_CR42) 1983; 28 1840_CR25 WE Kerr (1840_CR16) 1962; 70 GD Prestwich (1840_CR26) 1979; 5 JR Shorter (1840_CR35) 2012; 59 K Uematsu (1840_CR40) 2010; 20 HG Klemperer (1840_CR17) 1982; 7 A Tofilski (1840_CR39) 2008; 172 U Maschwitz (1840_CR18) 1974; 14 JO Schmidt (1840_CR31) 1983; 1 TM Nazareth (1840_CR22) 2010; 79 C Grüter (1840_CR12) 2012; 109 JS Zweden van (1840_CR41) 2011; 65 DW Roubik (1840_CR29) 2006; 37 C Bordereau (1840_CR4) 1997; 44 M Ono (1840_CR24) 1995; 307 |
References_xml | – reference: BrownRMDahlenEMillsCRickJBiblarzAEvaluation of an evolutionary model of self-preservation and self-destructionSuicide Life Threat19992958711:STN:280:DyaK1M3lsF2gsw%3D%3D – reference: SchmidtJOBlumMSOveralWLHemolytic activities of stinging insect venomsArch Insect Biochem1983115516010.1002/arch.940010205 – reference: KlempererHGParental behaviour in Copris lunaris (Coleoptera, Scarabaeidae): care and defence of brood balls and nestEcol Entomol1982715516710.1111/j.1365-2311.1982.tb00654.x – reference: BordereauCRobertATuyenVVPeppuyASuicidal defensive behaviour by frontal gland dehiscence in Globitermes sulphureus Haviland soldiers (Isoptera)Insect Soc19974428929710.1007/s000400050049 – reference: GrüterCMenezesCImperatriz-FonsecaVRatnieksFLA morphologically specialized soldier caste improves colony defense in a neotropical eusocial beeProc Natl Acad Sci U S A20121091182118632683332223268810.1073/pnas.1113398109 – reference: PrestwichGDChemical defense by termite soldiersJ Chem Ecol197954594801:CAS:528:DyaE1MXlt1Sls74%3D10.1007/BF00987930 – reference: DavidsonDWSalimKABillenJHistology of structures used in territorial combat by Borneo’s “exploding ants”Acta Zool20129348749110.1111/j.1463-6395.2011.00523.x – reference: NazarethTMMachadoGMating system and exclusive postzygotic paternal care in a Neotropical harvestman (Arachnida: Opiliones)Anim Behav20107954755410.1016/j.anbehav.2009.11.026 – reference: HermannHRSting autotomy, a defensive mechanism in certain social HymenopteraInsect Soc19711811112010.1007/BF02223116 – reference: JohnsonLKHubbellSPAggression and competition among stingless bees: field studiesEcology19745512012710.2307/1934624 – reference: SommeijerMJDistribution of labour among workers of Melipona favosa F.: age-polyethism and worker ovipositionInsect Soc19843117118410.1007/BF02232713 – reference: CouvillonMJWenseleersTImperatriz-FonsecaVLNogueira-NetoPRatnieksFLWComparative study in stingless bees (Meliponini) demonstrates that nest entrance size predicts traffic and defensivityJ Evol Biol2008211942011:STN:280:DC%2BD1c%2FgsFartA%3D%3D18021200 – reference: de CatanzaroDA mathematical model of evolutionary pressures regulating self-preservation and self-destructionSuicide Life Threat198616166181 – reference: SukaTInoueTNestmate recognition of the stingless bee Trigona (Tetragonula) minangkabau (Apidae: Meliponinae)J Ethol19931114114710.1007/BF02350047 – reference: WilleABiology of the stingless beesAnnu Rev Entomol198328416410.1146/annurev.en.28.010183.000353 – reference: NonacsPAlloparental care and eusocial evolution: the limits of Queller's head-start advantageOikos19912912212510.2307/3545413 – reference: Bates D, Maechler M, Bolker B, Walker S (2013) lme4: linear mixed-effects models using Eigen and S4. R package version. 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ZENODO. doi:10.5281/zenodo.12522 – reference: HuntGJGuzmán-NovoaEFondrkMKPageREQuantitative trait loci for honey bee stinging behavior and body sizeGenetics1998148120312131:CAS:528:DyaK1cXks1eit7c%3D14600549539435 – reference: SchmidtJOEvansDLSchmidtJOHymenopteran venoms: striving towards the ultimate defense against vertebratesInsect defenses: adaptive mechanisms of prey and predators1990AlbanyState University of New York Press387420 – reference: SefcKMMattersdorferKSturmbauerCKoblmüllerSHigh frequency of multiple paternity in broods of a socially monogamous cichlid fish with biparental nest defenceMol Ecol200817253125431:CAS:528:DC%2BD1cXotVOksLw%3D1843014610.1111/j.1365-294X.2008.03763.x – reference: Pinheiro J, Bates D, DebRoy S, Sarkar D and R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1-117 – reference: SeeleyTDHoneybee ecology: a study of adaptation in social life1985New JerseyPrinceton University Press – reference: van ZwedenJSGrüterCJonesSMRatnieksFLWHovering guards of the stingless bee Tetragonisca angustula increase colony defensive perimeter as shown by intra and inter-specific comparisonsBehav Ecol Sociobiol2011651277128210.1007/s00265-011-1141-2 – volume: 1 start-page: 155 year: 1983 ident: 1840_CR31 publication-title: Arch Insect Biochem doi: 10.1002/arch.940010205 – volume: 307 start-page: 334 year: 1995 ident: 1840_CR24 publication-title: Nature doi: 10.1038/377334a0 – volume: 59 start-page: 1 year: 2012 ident: 1840_CR35 publication-title: Insect Soc doi: 10.1007/s00040-011-0210-x – ident: 1840_CR25 – volume-title: R: a language and environment for statistical computing year: 2014 ident: 1840_CR27 – ident: 1840_CR3 – volume: 148 start-page: 1203 year: 1998 ident: 1840_CR14 publication-title: Genetics doi: 10.1093/genetics/148.3.1203 – volume: 37 start-page: 124 year: 2006 ident: 1840_CR29 publication-title: Apidologie doi: 10.1051/apido:2006026 – volume: 28 start-page: 536 year: 1980 ident: 1840_CR2 publication-title: Anim Behav doi: 10.1016/S0003-3472(80)80062-5 – volume: 7 start-page: 155 year: 1982 ident: 1840_CR17 publication-title: Ecol Entomol doi: 10.1111/j.1365-2311.1982.tb00654.x – volume-title: Honeybee ecology: a study of adaptation in social life year: 1985 ident: 1840_CR32 doi: 10.1515/9781400857876 – volume: 44 start-page: 289 year: 1997 ident: 1840_CR4 publication-title: Insect Soc doi: 10.1007/s000400050049 – volume: 79 start-page: 547 year: 2010 ident: 1840_CR22 publication-title: Anim Behav doi: 10.1016/j.anbehav.2009.11.026 – volume: 172 start-page: E239 year: 2008 ident: 1840_CR39 publication-title: Am Nat doi: 10.1086/591688 – volume: 76 start-page: 1653 year: 2008 ident: 1840_CR9 publication-title: Anim Behav doi: 10.1016/j.anbehav.2008.08.002 – volume: 18 start-page: 111 year: 1971 ident: 1840_CR13 publication-title: Insect Soc doi: 10.1007/BF02223116 – volume: 70 start-page: 190 year: 1962 ident: 1840_CR16 publication-title: J New York Entomol Soc – volume-title: The bees of the world year: 2000 ident: 1840_CR20 – volume: 51 start-page: 234 year: 2002 ident: 1840_CR38 publication-title: Behav Ecol Sociobiol doi: 10.1007/s00265-001-0429-z – volume: 109 start-page: 1182 year: 2012 ident: 1840_CR12 publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.1113398109 – start-page: 387 volume-title: Insect defenses: adaptive mechanisms of prey and predators year: 1990 ident: 1840_CR30 – volume: 21 start-page: 194 year: 2008 ident: 1840_CR8 publication-title: J Evol Biol doi: 10.1111/j.1420-9101.2007.01457.x – volume: 31 start-page: 171 year: 1984 ident: 1840_CR36 publication-title: Insect Soc doi: 10.1007/BF02232713 – ident: 1840_CR7 doi: 10.1016/0022-1910(95)00022-M – volume: 11 start-page: 141 year: 1993 ident: 1840_CR37 publication-title: J Ethol doi: 10.1007/BF02350047 – volume: 28 start-page: 41 year: 1983 ident: 1840_CR42 publication-title: Annu Rev Entomol doi: 10.1146/annurev.en.28.010183.000353 – volume: 70 start-page: 1331 year: 2005 ident: 1840_CR6 publication-title: Anim Behav doi: 10.1016/j.anbehav.2005.03.017 – volume: 16 start-page: 166 year: 1986 ident: 1840_CR11 publication-title: Suicide Life Threat doi: 10.1111/j.1943-278X.1986.tb00350.x – volume: 11 start-page: 317 year: 1964 ident: 1840_CR19 publication-title: Insect Soc doi: 10.1007/BF02227433 – volume: 17 start-page: 2531 year: 2008 ident: 1840_CR33 publication-title: Mol Ecol doi: 10.1111/j.1365-294X.2008.03763.x – volume: 29 start-page: 58 year: 1999 ident: 1840_CR5 publication-title: Suicide Life Threat doi: 10.1111/j.1943-278X.1999.tb00763.x – volume: 93 start-page: 487 year: 2012 ident: 1840_CR10 publication-title: Acta Zool doi: 10.1111/j.1463-6395.2011.00523.x – volume: 55 start-page: 120 year: 1974 ident: 1840_CR15 publication-title: Ecology doi: 10.2307/1934624 – volume: 20 start-page: 1182 year: 2010 ident: 1840_CR40 publication-title: Curr Biol doi: 10.1016/j.cub.2010.04.057 – volume-title: Animal behaviour year: 2005 ident: 1840_CR1 – volume: 110 start-page: 432 year: 1997 ident: 1840_CR21 publication-title: Oecologia doi: 10.1007/s004420050178 – volume: 29 start-page: 122 year: 1991 ident: 1840_CR23 publication-title: Oikos doi: 10.2307/3545413 – volume: 5 start-page: 459 year: 1979 ident: 1840_CR26 publication-title: J Chem Ecol doi: 10.1007/BF00987930 – volume: 217 start-page: 1059 year: 1982 ident: 1840_CR28 publication-title: Science doi: 10.1126/science.217.4564.1059 – ident: 1840_CR34 – volume: 14 start-page: 289 year: 1974 ident: 1840_CR18 publication-title: Oecologia doi: 10.1007/BF01039798 – volume: 65 start-page: 1277 year: 2011 ident: 1840_CR41 publication-title: Behav Ecol Sociobiol doi: 10.1007/s00265-011-1141-2 |
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SubjectTerms | aggression altruism Animal behavior Animal Ecology Apis mellifera appetite Bees Behavioral biology Behavioral Sciences Bioassays Biomedical and Life Sciences Brazil correlation defensive behavior Insects Life Sciences nesting nests Original Paper Pain predation probability stingless bees Suicide Teeth Trigona worker insects Zoology |
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Title | Appetite for self-destruction: suicidal biting as a nest defense strategy in Trigona stingless bees |
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