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 inBehavioral ecology and sociobiology Vol. 69; no. 2; pp. 273 - 281
Main Authors Shackleton, Kyle, Toufailia, Hasan Al, Balfour, Nicholas J., Nascimento, Fabio S., Alves, Denise A., Ratnieks, Francis L. W.
Format Journal Article
LanguageEnglish
Published Berlin/Heidelberg Springer 01.02.2015
Springer Berlin Heidelberg
Springer Nature B.V
Subjects
Online AccessGet full text
ISSN0340-5443
1432-0762
DOI10.1007/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.
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
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  givenname: Nicholas J.
  surname: Balfour
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  givenname: Fabio S.
  surname: Nascimento
  fullname: Nascimento, Fabio S.
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  givenname: Denise A.
  surname: Alves
  fullname: Alves, Denise A.
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  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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Issue 2
Keywords Nest guards
Stingless bees
Colony defense
Self-destructive behavior
Self-sacrifice
Trigona
Language English
License Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
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content type line 14
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Communicated by O. Rueppell
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PublicationTitle Behavioral ecology and sociobiology
PublicationTitleAbbrev Behav Ecol Sociobiol
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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
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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
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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
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LK Johnson (1840_CR15) 1974; 55
CD Michener (1840_CR19) 1964; 11
D Catanzaro de (1840_CR11) 1986; 16
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TD Seeley (1840_CR32) 1985
CD Michener (1840_CR20) 2000
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MJ Couvillon (1840_CR8) 2008; 21
T Suka (1840_CR37) 1993; 11
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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
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DW Roubik (1840_CR29) 2006; 37
C Bordereau (1840_CR4) 1997; 44
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– reference: MichenerCDReproductive efficiency in relation to colony size in hymenopterous societiesInsect Soc19641131734210.1007/BF02227433
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Snippet Self-sacrificial behavior represents an extreme and relatively uncommon form of altruism in worker insects. It can occur, however, when inclusive fitness...
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StartPage 273
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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