natural enemies of butterflies · 2020. 7. 19. · butterfly s/403986050 first instar of wanderer...
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Natural enemies of butterflies
Emeritus Professor Mike Keller
School of Agriculture, Food & Wine, Waite Campus
The University of Adelaide
What are the natural causes of mortality in butterflies?
• Host plants
• Predators
• Parasitoids Der
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Early mortality of Lepidoptera is high
M. P
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Causes of early mortality in Lepidoptera
• Predation and parasitism
• Physical factors (rain, wind)
• Host plant defenses
• Movement and failure to locate a host plant
Typical survival of early stages of Lepidoptera
Zalucki MP, Clarke AR, and Malcolm SB (2002) Ecology and behavior of first instar larval Lepidoptera. Annual Review of Entomology 47:361–93.
Eggs and first instars of wanderer butterfly suffer high rates of mortality
• Milkweeds produce toxic cardenolides that are concentrated in the milky sap.
• Even insects that specifically feed on milkweeds can be adversely affected by these toxins
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Egg of wanderer butterfly
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05
0
First instar of wanderer butterfly
Pad
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Survival of first instar wanderer butterfly is affected by plant species and latex sap
0 20 40 60 80
A. syriaca
A. curassavica
A. incarnata
A. eriocarpa
A. fruticose
A. tuberosa
A. humistrata
A. californica
A. erosa
% Survival
Intact Severed
Common milkweed A. syriaca
Der
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Pathogens
• Caper white, Belenois java, can be infected by a virus
Insectivorous birds
Willie wagtail
Dav
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NC
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s/ko
okr
/70
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07
72
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Superb fairy wren
Ben
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44
, (C
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com
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File
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New Holland honeyeater
JJ H
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son
, (C
C B
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A 2
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Spiders Crab spiders (Thomisidae)
ambush flower visitors
Vin
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Ker
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Spiders
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11
97
99
Jumping spider, Simaethula sp.
Wolf spider Venator spenceri
Rez
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Cat
her
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Her
ms,
Th
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St
ate
Un
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sity
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Jumping spider attacking butterfly
Jumping spiders, Salticidae
Dav
id C
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aert
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Predatory bugs
Oechalia schellenbergii
Rez
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Nabis kinbergii
Ton
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A pentatomid
DBM
Positive control
DBM DBM Pieris
Negative crl.
Detection of prey DNA in gut contents of predators
Rez
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th
esis
0
0.1
0.2
0.3
0.4
0.5
0.6
Nabid Wolf Spider
Brown Lacewing
Ladybird Carabid Other Spider
Staphylinid
De
tec
tio
n o
f D
BM
Consumption of diamondback moth by predators
What is a parasitoid?
• Larvae of a parasitoid feed on and develop in association with a single host insect and usually kill it.
• All insect parasitoids are holometabolous – their development includes egg, larval, pupal and adult stages
Cotesia glomerata stinging a larva of Peiris rapae
Cotesia rubecula (Hymeoptera: Braconidae)
Types of parasitism
• Ectoparasitism - larvae develop externally, usually with their mouthparts buried in the body of their host
• Endoparasitism - larvae feed and develop within the body of their host
M. K
elle
r Ectoparasitoid: Larvae of the wasp Euplectrus agaristae parasitising a larva of the grapevine moth
M. K
elle
r
Endoparasitoid: Larva of the wasp Cotesia rubecula parasitising a larva of Pieris rapae
Types of parasitism
• Idiobiont - host development is arrested by oviposition
• The food resources available to the parasitoid are fixed
• Koinobiont - hosts to continue to develop after oviposition
• Host development can extend the amount of food available to the developing parasitoid
Trichogramma exiguum
parasitises the eggs of
Lepidoptera. It is an
idiobiont.
Sourc
e:
M.
S. T
hom
son
Modes of parasitism
Solitary vs. gregarious parasitoids
• Solitary parasitoids – only one individual normally develops in one host
• Gregarious parasitoids – more than one parasitoid normally parasitises one host
• Superparasitism – more parasitoids attack a host than can normally develop on it
• Multiparasitism – a host is parasitised by more than one species
• Hyperparasitism – a parasitoid is parasitised by another parasitoid
Taxonomic range of parasitoid insects
Raphidioptera
Magaloptera
Neuroptera
Coleoptera
Strepsiptera
Symphyta
Orussidae
Apocrita
Mecoptera
Siphonaptera
Endopterygota [Holometabola]
Hymenoptera
Coleopterida
Neuropterida
Panorpida
Trichoptera
Lepidoptera
Diptera
Groups that contain parasitoids are shown in blue
Hymenoptera: Apocrita
• This is the most diverse group of insects!
Sou
rce:
agr
esea
rch
mag
.ars
.usd
a.go
v
Pteromalus puparum on fly puparium
Spathius galinae parasitises the larvae of emerald ash
borer inside ash trees
Sou
rce:
Jia
n D
uan
Sou
rce:
USD
A
Trichogramma pretiosum Parasitising lepidopteran egg
Sou
rce:
new
s.sc
ien
ce3
60
.go
v
Aphidius ervi parasitising an aphid
Trichogramma exiguum
parasitises the eggs of
Lepidoptera. It is about
0.5 mm long!
Photo
: M
. S
. T
hom
son
Euplectrus agaristae is
an external parasitoid
of grapevine moth
Orgilus lepidus parasitises
larval potato tuber moth
Parasitic Diptera
• ~16,000 described species of Diptera are parasitoids
• Parasitoid lifecycle has evolved >100 times in Diptera!
Eggs of a tachinid on a lepidopteran larva
Sou
rce:
Un
iv. o
f C
alif
orn
ia
Voria ruralis (Tachinidae) parasitises lepidopteran larvae
Sou
rce:
hed
y24
11
Sou
rce:
Cla
rice
L1
L2
L3 L4
Adult Trichogramma carverae
Dolichogenidea tasmanica
Therophilus unimaculatus
Voriella uniseta
Brachymeria phya
Pupa Egg
L6
L5
Parasitoids of Epiphyas postvittana
Hymenopteran reproduction
• Many species exhibit haplodiploid reproduction • Females are diploid • Males are haploid
• Females control the sex of offspring by choosing to fertilise eggs when laying them
• Often sex ratios are biased toward females.
Complementary sex determination
• Species have several to many sex-determining alleles
• If any sex allele is heterozygous, then the offspring is female
• If all sex alleles are homozygous or hemizygous, then the offspring are male
• Diploid males typically don’t develop to maturity; those that do develop are sterile
What factors influence the searching behaviour of parasitic wasps?
Chemical Messengers
Hormones
(Inside individuals)
Semiochemicals
(Between individuals)
Pheromones
(Within species) (Between species)
Kairomones
(- emitter, + receiver)
Synomones
(+ emitter, + receiver)
Allomones
(+ emitter, - receiver)
Host selection by parasitoids
Host habitat location
Host location
Host acceptance
Host regulation
Non-contact cues
Contact cues
Nu
mb
er a
nd
inte
nsi
ty o
f cu
es
Experiments on the behavior of parasitoids
Navigation in flying insects
DO
I:1
0.4
319
/lo
.20
01.4
6.5
.103
4
Odour plume In a wind tunel
Wind
Anemotaxis
Intrinsic
factors
Extrinsic
factors
Host density
Host
distribution
Host stage
Age
Energy
reserves
Experience
/learning Infochemicals
Parasitism
Host plant
Host plants, predators and parasitoids threaten the survival of butterflies
Der
ek R
amse
y, G
NU
FD
L 1
.2
Ton
y B
aile
y, l
epid
op
tera
.bu
tter
flyh
ou
se.c
om
.au
/nym
p/p
lexi
pp
us.
htm
l
Sou
rce:
M. S
. Th
om
son
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