A Wandering Monarch in a
Milkweed Patch: some ideas for
butterfly conservation.
Myron (‘Meron’) P. Zalucki
School of Integrative Biology
The University of Queensland, Australia
Acknowledgments
Lincoln Brower, Mike Bull, Tony Clarke, Hugh Dingle, Jane
Hughes, Roger Kitching, Duncan Mackay, Steve Malcolm,
Tim Paine, Wayne Rochester, Yoshito Suzuki, … and many
others
Monarchs “down-under”
Applied entomology
Basic entomology
Will monarchs go
extinct ?
Already an endangered
phenomenon! Will Bt corn,
climate change, & herbicides
impact on monarchs?
Climate & changes in abundance
Milkweed abundance at a
landscape level & host plant
search - metapopulations &
habitat
Modelling risk…
What determines large scale
fluctuations in monarch
abundance?
Climate...
• Affects milkweed
• Affects reproduction & survival
• Will have a strong influence on seasonal & year to
year abundance & distribution
+
-
D.plexippus
D.petilia
in North America
Year to year variation in climatic suitability
Expect large scale variation in abundance…
The distribution and abundance of host plant
patches will have a dramatic effect on monarch
abundance
Milkweed
Metapopulation of interconnected milkweed patch ‘habitats’
Habitat?
Milkweed patch and
surrounding ‘highish’
density of single plants
defines breeding habitat.
Metapopulation of interconnected milkweed patch ‘habitats’
Space between is NOT
empty!
Rules for egg laying
If (‘habitat’) lay all eggs
If (‘not habitat’) depends on isolated plants found
Monarch Reproduction
And that all depends on distribution and abundance
of milkweed and the monarchs ability to find these
Eggs / female / day
80
60
40
20
0
0
100
200
300
400
500
600
Age in Degree days (dz=11.5 oC)
Zalucki. 1981. Res Pop Ecol 23: 318 - 27
What happens as the single plant density
(SPD) increases in non-patch areas?
SPD = 0.01
Proportion of eggs laid as single plant density
(SPD) increases in non-patch areas
Search parameter same for patches and singles
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.45
0.2
1
0.4
0.75
0.1
0.5
0
0.35
0.25
0.1
0.25
0.05
0.5
0.75
0.3
0
1
2
4
0.25
0.2
0.15
SPD = 0.1
0.1
1
0.05
0.9
0
0.8
4
0.7
2
0
1
0.6
0.05
0.25
0.75
0.5
0.5
0.75
0.25
0.5
0.1
1
0.4
0.3
0.2
1
0.75
0.1
Change in Proportion eggs laid
0.5
0
0.25
0.1
0.25
0.05
0.5
0.75
0
1
2
4
0.2
0.18
SPD = 0.2
0.16
0.14
1
0.12
0.9
0.8
0.1
0.7
0.08
0.6
0.06
0.5
0.04
0.4
0.02
0
0.3
0.2
1
0.75
0.1
0.5
0
0.25
0.1
0.25
0.05
0.5
0.75
1
0
2
4
4
2
0
1
0.05
0.25
0.75
0.5
0.5
0.75
0.25
0.1
1
Returns on eggs will
depend on factors
affecting immature
monarch survival
Zalucki, Clarke & Malcolm
Ann Rev Ent 47: 361-393
Earlystage
stage monarch
survival
Early
survival
& patch
size: egg to II instar
Patches: 10%
Singles: 20%
1
0.75
0.5
Predators?
0.25
0
egg
I
Stage
II
Large larval survival:
III to V instar
Patch plants
Single plants
50%
33%
Food limitation?
Parasitism levels
range from
11-80 % in
winter/spring
to
38-99.9 % in
summer/autumn
Patch plants 58%
Single plants 36%
So putting eggs on
single plants gives a
higher return…
Random search for singles
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
1000
0
Population persistence
depends very much on
ability to find plants both
as patches & singles
250
0
0.1 0.25
0.5
0.75
100
1
2
4
Proportion landscape with
milkweed patch habitat
1.8
1.6
NRR
1.4
1.2
1
0.8
0.6
0.4
0.2
1000
0
0
250
0.1 0.25
0.5
0.75
1
100
2
4
Density of single plants
outside milkweed patch
habitat
Population viability analysis of migratory monarch
butterflies exposed to genetically modified maize
Continental-scale resource use
migration
Malcolm,
Cockrell, &
Brower, 1993
Primary target of GM Bt-maize is the
European corn borer
http://www.ent.iastate.edu/pest/cornborer/intro/intro.html
Non-target effects of
Bt-maize pollen:
• Losey, Rayor & Carter, 1999.
Nature 399: 214.
– Larval mortality increased 44%
in greenhouse.
• Hansen Jesse & Obrycki.
2000. Oecologia 125: 241248.
– 17-20% increase in mortality of
larvae exposed in the
laboratory to Bt corn pollen
deposited naturally on A.
syriaca leaves.
Risk assessment
• Sears et al. 2001 (PNAS 98) measured risk in Iowa as:
– R = Pe x Pt
• Risk = probability of exposure x probability of toxic effect
– For Bt176 pollen:
• R = 0.0042 x 0.9 = 0.0038
(0.38%)
– For Mon810 and Bt11 pollen:
• R = 0.0168 x 0.007 = 0.00012
(0.012%)
– At 80% adoption this becomes:
• R = 0.067 x 0.007 = 0.00047
(0.047%)
• These estimates of R were revised by Dively et al. 2004
(Environ. Entomol. 33) to:
– At 37% Bt corn use in Iowa, R = 0.0124
(1.24%)
• mortality of 2nd generation in Iowa.
– At maximum 80% Bt corn use, R = 0.0261
(2.6%)
• Where Pe = proportion monarchs from maize (l) x overlap of pollen shed (o) x
adoption rate of Bt maize (a).
What does this ‘low’ risk mean for
monarch butterflies?
– Gi = (Gi-1Ri + iGi-2Ri)SeSlSp
• G = generation size.
• = proportion overlap
varies from 0 to 0.1.
• R = average realized
fecundity.
• S = survivorship of eggs,
larvae & pupae.
G4
G3
latitude
• We use the risk measures
for monarch generation 2
of Dively et al. 2004 in a
spatially discrete model of
4 linked generations
where:
G2 G3=Bt
G1
spring migration
overwintering
time
autumn
migration
Stochastic density independent models
were run for 100 simulations of 100 years
Mexico
Mexico
450000000
120000000
400000000
100000000
350000000
80000000
250000000
Mexico
200000000
150000000
Number
Number
300000000
60000000
Mexico
40000000
100000000
20000000
50000000
0
0
1
7
13
19
25
31
37
43
49
55
61
67
73
79
85
91
97
Year
Model 1 with random normally varying
reproduction and no Bt corn effect on
survival in G3
with variable generation overlap
[R = Pe x Pt = 0.0 x 0.07 = 0.0]
mean = 0/500 OW<500,000 (N=100)
1
7
13
19
25
31
37
43
49
55
61
67
73
79
85
91
97
Year
Model 1 with random normally varying
reproduction and Bt corn effect on
survival in G3 and effect on
reproduction in G4
with variable generation overlap
[R = Pe x Pt = 0.024 x 0.07 = 0.002]
mean = 0/500 OW<500,000 (N=100)
% extinction at overwintering threshold of
1 million monarchs vs exposure to Bt maize
Percentage of simulations in which N fell below threshold
100%
Density independent
model 1
no
no overlap
carryover
90%
80%
Percentage
70%
60%
50%
40%
30%
20%
10%
carryover
+ 50%
10%
overlap
+
10%
50% fecundity reduction
0%
0
0.05
0.1
0.15
0.2
0.25
Pe (Proportion exposed to Bt) in DI Random 1
Percentage of simulations in which N fell below theshold
Density dependent
model 4
90%
nooverlap
carryover
no
80%
Percentage
70%
60%
50%
40%
30%
20%
10% overlap
carryover++50%
50% fecundity
reduction
10%
fecundity
reduction
10%
0%
0
0.05
0.1
0.15
Pe (Proportion exposed to Bt) in DD Random 4
0.2
0.25
Will monarchs go extinct?
• During the 2004/5 winter monarch overwintering
populations were the lowest recorded at 2.1 ha of
overwintering forest in Mexico.
– 10% of the largest recorded area of 21 ha in 1996/97.
Overwintering colony areas (hectares)
(redrawn from Rendon and Galindo-Leal, 2005)
22
Number of hectares
20
18
16
14
12
10
8
6
4
2
0
93-94
94-95
95-96
96-97
97-98
98-99
99-00
00-01
Overwintering season
01-02
02-03
03-04
04-05
Will monarchs go extinct?
• The conclusion of Sears
et al. 2001 and Dively
et al. 2004 that Bt
maize poses low risk to
monarchs is premature.
• Require more spatially
and temporally relevant
life-history data before
reaching a conclusion.
Will monarchs go extinct?
• Need to determine the impact
of added mortality from GM
crops on the population
dynamics of monarchs.
• A range of simulations suggests
that the impact of Bt maize is
not trivial.
• We also propose to address the
impact of herbicide-tolerant
soya beans.
Will monarchs go
extinct ?
Don’t know … will
depend in part on
climate & host
plant distribution
across the
Landscape & risks
For this wanderer in a milkweed patch