Biol 316 Invertebrate Zoology

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Biol 316 - Invertebrate Zoology
Anne Gaskett agaskett_at_bio.mq.edu.au

• Animal Communication 2
• Signal Costs Exploitation

Image Simone Cottrell Botanic Gardens Trust
2
todays lecture
1. Signal constraints costs - handicap
hypothesis - costs, tradeoffs cheating 2.
Exploitation - eavesdropping - signal biases -
mimicry deception sexually deceptive orchids
3
todays lecture
1. Signal constraints costs - handicap
hypothesis - costs, tradeoffs cheating 2.
Exploitation - eavesdropping - signal biases -
mimicry deception sexually deceptive orchids
4
signal constraints
Environmental conditions e.g. forest structures
can influence transmission of auditory
signals Receiver psychology ability of the
receiver to detect and recognise types of
signals Emitter physiology, ecology
condition ability of the emitter to produce the
signal and bear the associated costs
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costs of signalling
signal production can be costly

• Pea aphids produce alarm pheromones from
  compounds usually involved in juvenile hormone
  synthesis

• immature aphids that produce lots of alarm
  pheromone must delay reproduction

Acyrthosiphon pisum www.ento.csiro.au
Mondor Roitberg 03 Age-dependent fitness costs
of alarm signaling in aphids Can J Zool 81757-62
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costs of signalling
some male wolf spiders drum their abdomen on
dry leaves during courtship females prefer fast
drummers
Hygrolycosa rubrofasciata http//www.cc.jyu.fi/
Kotiaho et al. measured male CO2 production
during resting, drumming, moving maximal
exertion Drumming required 22 times more energy
than resting, and twice the energy of maximal
exertion!
Kotiaho et al. 98 Energetic costs ofsexual
signalling in a wolf spider Proc R Soc Lond B
2652203-9
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todays lecture
1. Signal constraints costs - handicap
hypothesis - costs, tradeoffs cheating 2.
Exploitation - eavesdropping - signal biases -
mimicry deception sexually deceptive orchids
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the handicap hypothesis

• Sometimes the high cost of a signal is why it is
  used.
• Expensive signals indicate that the signaller is
  of high quality can afford the energy
  expenditure
• handicap hypothesis (Zahavi 1975 Theor.
  Biol.)

orthe bling hypothesis (The BG, Juvenile,
Lil Wayne, Turk Baby Mannie Fresh 1999 Cash
Money Records)
From http//en.wikipedia.org/wiki/Bling
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the handicap hypothesis

• For signals that indicate the quality of the
  emitter
• Explains that
• when signals are honest,
• 2) high signal cost ensures the signal reliably
  indicates emitters quality as a mate/competitor
  etc.
• 3) Often a direct link between the signal mode
  and the quality being signalled.
• Dishonesty is tolerable if its infrequent

Zahavi 1975
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the handicap hypothesis

• e.g. Immunocompetence handicap hypothesis
• For males, more testosterone allows more
  fighting, calling ornaments (often attractive
  to females)
• but alsoimpairs male immune function
• Only the healthiest males can afford
  impressive calling, ornaments etc.
• But does the data support this?
• More info? See Roberts et al. 2004 Testing the
  immunocompetence handicap hypothesis a review of
  the evidence Anim Behav 68227-239

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todays lecture
1. Signal constraints costs - handicap
hypothesis - costs, tradeoffs cheating 2.
Exploitation - eavesdropping - signal biases -
mimicry deception sexually deceptive orchids
12
costs tradeoffs
Horn expression in Dung beetles
Male Onthophagus sp. can have horns on the front,
middle or back of their head or on the thorax
http//dbs.umt.edu/research_labs/emlenlab/project1
.htm
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costs tradeoffs
Males with larger horns have smaller eyes,
antennae or wings depending on horn location
Horns grow when males are juveniles and have
limited food tradeoff between sizes of body
parts suggests having horns is costly
http//dbs.umt.edu/research_labs/emlenlab/project1
.htm
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costs tradeoffs

• can minimise costs by modulating or modifying
  signals

Female St Andrews Cross spiders (Argiope
keyserlingi) emit chemical signals to attract
males
But males exert costs steal food, hinder prey
capture, and attract predators
after mating, females stop emitting chemical
attractant
Herberstein et al. 2002 Costs of courtship and
mating in a sexually cannibalistic orb-web
spider, Behav Ecol Sociobiol 51440 - 446
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dishonest signals

• Can cheat costs with dishonest signalling

Male Uca annulipes crab threatens opponents with
one enlarged chelicera - Forelimb size is an
honest signal of threat
Male still signals if his chelicera is weak
flimsy after regrowth
Uca sp.
-- may deter opponents avoid conflict, but if
challenged, risks losing contest and being killed
Blackwell et al. 2000 Dishonest signalling in a
fiddler crab Proc Roy Soc Lond B 267719-724
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dishonest signals

• Batesian mimicry
• Harmless species mimic features of toxin
  producing species and avoid predation

• Perfect or specific mimicry by Syrphids
  (hoverflies)

Hoverfly mimic
model
model
Hoverfly mimic
Sericomyia silentis www-biol.paisley.ac.uk
Volucella bombylans insektenfotos.de/
Bombis terrestris insektenfotos.de/
Vespa crabro www.david.element.ukgateway.net
Edmunds 2000 Why are there good and poor mimics?
Biol J Linn Soc 70459-466
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dishonest signals

• Batesian mimicry

Imperfect or general mimicry is much more common
Why?
Hoverfly general mimics
Syrphus ribesii insektenfotos.de/
Episyrphus balteatus insektenfotos.de/
Eristalis intricarius www.wildlife.shetland.co.uk
Edmunds 2000 Why are there good and poor mimics?
Biol J Linn Soc 70459-466
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todays lecture
1. Signal constraints costs - handicap
hypothesis - costs, tradeoffs cheating 2.
Exploitation - eavesdropping - signal biases -
mimicry deception sexually deceptive orchids
19
exploitation

• a major cost of using signals is the risk of
  exploitation by another species
• eavesdropping parasites or predators
• exploitation of sensory biases
• mimicry for deception

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exploitation via eavesdropping
Teleogryllus oceanicus Robert Wyttenbach
www.nbb.cornell.edu
Male crickets calls attract females indicate
male quality T. oceanicus females prefer long
chirps but parasitoid wasps also use
long chirps to find male T. oceanicus in which
to lay their eggs - tradeoff between
attracting females parasitoids
Simmons et al. 01 Geographic variation in female
preference functions male songs of the field
cricket Teleogryllus oceanicus Evolution,
551386-94
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todays lecture
1. Signal constraints costs - handicap
hypothesis - costs, tradeoffs cheating 2.
Exploitation - eavesdropping - signal biases -
mimicry deception sexually deceptive orchids
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exploitation of signal biases
All animals have sensory or signal biases due to
receiver psychology coevolution - Sometimes
called a sensory trap
e.g. Australian Crab spiders exploit honeybees
bias for floral UV signals (Described in
Mariellas lecture on foraging)
Heiling et al. 2003 Crab spiders manipulate
flower signals Nature 421 334
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exploitation of signal biases
Do nuptial gifts exploit female sensory bias for
food?

• When courting a female, some male spiders
  insects give food (nuptial gifts)
• Why?
• as a signal of males quality as a mate?
• to increase female fecundity (direct benefit)?
• to provide in-direct benefits to offspring?
• as a sensory trap?

Karim Vahed (2007) All that glisters is not gold
sensory bias, sexual conflict nuptial feeding
in insects spiders Ethology 113105-127
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exploitation of signal biases

• Vahed (2007) argues that food gifts are a sensory
  trap
• Exploits strong selection for female interest in
  food
• Distracts females so males can control
  copulation duration sperm transfer.

No evidence gifts provide direct or indirect
benefits (gifts dont affect female fecundity or
offspring health) Some evidence that gifts allow
males control (in general, males with gifts get
more matings, mate for longer transfer more
sperm)
Karim Vahed (2007) All that glisters is not gold
sensory bias, sexual conflict nuptial feeding
in insects spiders Ethology 113105-127
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todays lecture
1. Signal constraints costs - handicap
hypothesis - costs, tradeoffs cheating 2.
Exploitation - eavesdropping - signal biases -
mimicry deception sexually deceptive orchids
26
mimicry deception
(Z)-7-dodecenyl acetate
plus females of 136 other moth species
Rasmussen et al. 1996 Insect pheromone in
elephants Nature 379684
Chemical signals - often similar between
species - are extremely compelling for the
receiver good fodder for the evolution of
mimicry deception!
Images hortipm.tamu.edu/pestprofiles
ukmoths.org.uk www.zlutejslon.cz/namalujte_sloni.h
tml mothphotographersgroup.msstate.edu
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mimicry deception
Ants have colony-specific cuticular scents - can
recognise nest mates intruders
Yet Cosmophasis bitaeniata jumping spiders live
in weaver ant nests and prey on ant larvae
Oecophylla smaragdina wikipedia.com
www.salticidae.org
Allan et al. 2002 Mimicry of host cuticular
hydrocarbons by salticid J Chem Ecol 28835-48
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mimicry deception
Do spiders mimic ant pheromones?

• wash ants and spiders in solvent
• identify compounds
• - spider larval ant scent is similar
• behavioural assays with adult ants solvent
  extracts
• - adult ants dont attack spider or larval
• scent

Adult ant
Larval ant
Spider
Allan et al. 2002 Mimicry of host cuticular
hydrocarbons by salticid J Chem Ecol 28835-48
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mimicry deception
Many female insects attract males with sex
pheromones ( signal)
Male insects use sex pheromone signals plus cues
such as shapes, colours and textures to find and
choose females
But sexually deceptive orchids mimic these
signals and cues to lure pollinators
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mimicry deception
Orchid pollen
Chiloglottis orchids fool male thynnine wasps
into gripping flower attempting
copulation Hinged petal slams male into orchid
pollen Male delivers pollen next time he is
fooled
Hinged petal
Peakall
Wong et al. 04 Pollinator attractiveness
increases with distance...Proc R Soc Lond B
(Suppl) 271S212-4
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mimicry deception
Is deception by orchids costly to
pollinator? Most experts say no Sexual
deception has little impact on pollinators
(Dafni 1987 Peakall 1990 Schiestl 2005
Jersakova et al. 2006) But do male insects waste
time energy copulating with orchids? Do female
male insects miss mating opportunities? Do male
insects waste sperm on orchids?
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Australian Sexually Deceptive Cryptostylis
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Movies by Bonnie Dalrymple (Undergrad) Claire
Winnick (Research Assistant)
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Pollinator - Male wasp (Lissopimpla excelsa)
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Dissection of male repro organs
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Male wasp sperm from dissected testes
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Male wasp sperm from dissected testes after
staining with fluorescent dye
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Collected Cryptostylis orchids from uni Ecology
Reserve
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Took orchids to new site, recorded when wild
wasps copulated with flowers Rushed flowers to
lab for microscopy
Marnie Innis watches an orchid flower for insect
copulations
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Mysterious blob
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Blobs left on orchid flowers after pollination
contained stacks of sperm!
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73 of orchid copulations involve ejaculation!
(n26)
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Costs of deception ejaculation

• Cost of producing the sperm
• Sperm production can be costly for insects

• Missed mating opportunities
• If males have no sperm left after orchid visit
• or if refractory period until male can make
  more sperm

• Disadvantaged in sperm competition?
• Can sperm depleted males transfer enough sperm to
  compete against other males sperm in female
  tracts?

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Could these costs drive evolution of insect
ability to learn to recognise and avoid
orchids? Is this in turn selecting for
increasingly sophisticated orchid mimicry? Do we
have the first compelling evidence of
antagonistic coevolution or an arms race between
orchids and their pollinators?
Look for us in press this year Gaskett, Winnick
Herberstein (2008) Orchid sexual deceit
provokes pollinator ejaculation American
Naturalist
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Are Cryptostylis orchids winning the arms race?
plants pollinated per season for sex.deceptive
orchids
European Ophrys spp 22.81
Drakaea glyptodon 202
Leporella fimbriata 23.53
Chiloglottis trilabra 414
Cryptostylis spp. 645
1Neiland Wilcock 98wikipedia.org 2Peakall
90 www.caladenia.net 3Peakall 89Heberle,
Species Orchid Soc WA 4Peakall Handel
93Peakall 5 Gaskett Herberstein 05Schiestl
et al. 04
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todays lecture
1. Signal constraints costs - handicap
hypothesis - costs, tradeoffs cheating 2.
Exploitation - eavesdropping - signal biases -
mimicry deception sexually deceptive orchids
47
Some sources for more information
David Attenborough/BBC Life in the Undergrowth
series Schiestl 2005 On the success of a
swindle pollination by deception in orchids
Naturwissenschaften 92(6)255-264 If interested
email me for PDFs agaskett_at_bio.mq.edu.au