Paper · 2018 · Journal of Animal Ecology

Elevated atmospheric carbon dioxide concentrations promote ant tending of aphids

Jenni M. M. Kremer; Sabine S. Nooten; James M. Cook; et al.

7
claims
18
verbatim quotes
24
citations
2
research areas
✓
Open access

Abstract

Abstract Animal mutualisms, which involve beneficial interactions between individuals of different species, are common in nature. Insect–insect mutualism, for example, is widely regarded as a keystone ecological interaction. Some mutualisms are anticipated to be modified by climate change, but the focus has largely been on plant–microbe and plant–animal mutualisms rather than those between animals. Ant–aphid mutualisms, whereby ants tend aphids to harvest their honeydew excretions and, in return, provide protection for the aphids, are widespread. The mutualism is heavily influenced by the quality and quantity of honeydew produced by aphids, which is directly affected by host plant quality. As predicted increases in concentrations of atmospheric carbon dioxide ( eCO 2 ) are widely reported to affect plant nutritional chemistry, this may also alter honeydew quality and hence the nature of ant–aphid mutualisms. Using glasshouse chambers and field‐based open‐top chambers, we determined the effect of eCO 2 on the growth and nutritional quality (foliar amino acids) of lucerne ( Medicago sativa ). We determined how cowpea aphid ( Aphis craccivora ) populations and honeydew production were impacted when feeding on such plants and how this affected the tending behaviour of ants ( Iridomyrmex sp.). eCO 2 stimulated plant growth but decreased concentrations of foliar amino acids by 29% and 14% on aphid‐infested plants and aphid‐free plants, respectively. Despite the deterioration in host plant quality under eCO 2 , aphids maintained performance and populations were unchanged by eCO 2 . Aphids induced higher concentrations of amino acids (glutamine, asparagine, glutamic acid and aspartic acid) important for endosymbiont‐mediated synthesis of essential amino acids. Aphids feeding under eCO 2 also produced over three times more honeydew than aphids feeding under ambient CO 2 , suggesting they were imbibing more phloem sap at eCO 2 . The frequency of ant tending of aphids more than doubled in response to eCO 2 . To our knowledge, this is the first study to demonstrate the effects of atmospheric change on an ant–aphid mutualism. In particular, these results highlight how impending changes to concentrations of atmospheric CO 2 may alter mutualistic behaviour between animals. These could include positive impacts, as reported here, shifts from mutualism to antagonism, partner switches and mutualism abandonment.

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Claims 7

Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Elevated CO2 stimulated lucerne growth.

Taxon
lucerneMedicago sativae1
Treatment
eCO 2e0
Outcome
plant growthe0
Direction
stimulatede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Medicago sativa
Medicago sativa · TaxonDrepanostoma · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“eCO 2 stimulated plant growth”

✓ located verbatim in the source · abstract, characters 1310–1339 · show in text ↑
e1

“lucerne ( Medicago sativa )”

✓ located verbatim in the source · abstract, characters 1079–1106 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Elevated CO2 lowered foliar amino acids by 29% in aphid-infested lucerne.

Taxon
lucerneMedicago sativae2
Treatment
eCO 2e1
Interactor
aphide0pest
Outcome
concentrations of foliar amino acidse0
Direction
decreasede0
Value
29%e0
Qualifier
aphid‐infested plantse0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Medicago sativa
Medicago sativa · TaxonDrepanostoma · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“decreased concentrations of foliar amino acids by 29% and 14% on aphid‐infested plants and aphid‐free plants, respectively”

✓ located verbatim in the source · abstract, characters 1344–1466 · show in text ↑
e1

“eCO 2 stimulated plant growth”

✓ located verbatim in the source · abstract, characters 1310–1339 · show in text ↑
e2

“lucerne ( Medicago sativa )”

✓ located verbatim in the source · abstract, characters 1079–1106 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Elevated CO2 lowered foliar amino acids by 14% in aphid-free lucerne.

Taxon
lucerneMedicago sativae2
Treatment
eCO 2e1
Outcome
concentrations of foliar amino acidse0
Direction
decreasede0
Value
14%e0
Qualifier
aphid‐free plantse0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Medicago sativa
Medicago sativa · TaxonDrepanostoma · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“decreased concentrations of foliar amino acids by 29% and 14% on aphid‐infested plants and aphid‐free plants, respectively”

✓ located verbatim in the source · abstract, characters 1344–1466 · show in text ↑
e1

“eCO 2 stimulated plant growth”

✓ located verbatim in the source · abstract, characters 1310–1339 · show in text ↑
e2

“lucerne ( Medicago sativa )”

✓ located verbatim in the source · abstract, characters 1079–1106 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Cowpea aphid populations were unchanged under elevated CO2.

Taxon
lucerneMedicago sativae2
Treatment
eCO 2e0
Interactor
cowpea aphidAphis craccivorae1pest
Outcome
populationse0
Direction
unchangede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Medicago sativa
Medicago sativa · TaxonDrepanostoma · CC BY 4.0 · iNaturalist ↗
Aphis craccivora
Aphis craccivora · InteractorSimon Hinkley & Ken Walker Museum Victoria · CC BY 3.0 au · Wikimedia Commons ↗

Verbatim

e0

“aphids maintained performance and populations were unchanged by eCO 2”

✓ located verbatim in the source · abstract, characters 1530–1599 · show in text ↑
e1

“cowpea aphid ( Aphis craccivora )”

✓ located verbatim in the source · abstract, characters 1126–1159 · show in text ↑
e2

“lucerne ( Medicago sativa )”

✓ located verbatim in the source · abstract, characters 1079–1106 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Aphid infestation induced higher levels of four amino acids in lucerne.

Taxon
lucerneMedicago sativae1
Treatment
Aphidse0
Interactor
AphidsAphidomorphae0pest
Outcome
concentrations of amino acids (glutamine, asparagine, glutamic acid and aspartic acid)e0
Direction
highere0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Medicago sativa
Medicago sativa · TaxonDrepanostoma · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“Aphids induced higher concentrations of amino acids (glutamine, asparagine, glutamic acid and aspartic acid)”

✓ located verbatim in the source · abstract, characters 1602–1710 · show in text ↑
e1

“lucerne ( Medicago sativa )”

✓ located verbatim in the source · abstract, characters 1079–1106 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Aphids feeding under elevated CO2 produced over three times more honeydew than at ambient CO2.

Taxon
lucerneMedicago sativae1
Treatment
eCO 2e0
Interactor
AphidsAphidomorphae0pest
Outcome
Aphids feeding under eCO 2 also produced over three times more honeydewe0
Direction
moree0
Value
over three timese0
Comparator
ambient CO 2e0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Medicago sativa
Medicago sativa · TaxonDrepanostoma · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“Aphids feeding under eCO 2 also produced over three times more honeydew than aphids feeding under ambient CO 2”

✓ located verbatim in the source · abstract, characters 1783–1893 · show in text ↑
e1

“lucerne ( Medicago sativa )”

✓ located verbatim in the source · abstract, characters 1079–1106 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Ant tending of aphids more than doubled under elevated CO2.

Taxon
lucerneMedicago sativae1
Treatment
eCO 2e0
Interactor
aphidsAphidomorphae0pest
Second interactor
antsFormicidaee2other
Outcome
frequency of ant tending of aphidse0
Direction
doublede0
Value
more than doublede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Medicago sativa
Medicago sativa · TaxonDrepanostoma · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“The frequency of ant tending of aphids more than doubled in response to eCO 2”

✓ located verbatim in the source · abstract, characters 1953–2030 · show in text ↑
e1

“lucerne ( Medicago sativa )”

✓ located verbatim in the source · abstract, characters 1079–1106 · show in text ↑
e2

“ants ( Iridomyrmex sp.)”

✓ located verbatim in the source · abstract, characters 1285–1308 · show in text ↑

co2 · molecular: metabolites · Medicago sativa (alfalfa)Positive and negative results

5 papers: 2 positive, 3 negative or no effect

2 papers in the same direction as this paper · 2 in the opposite direction

  1. positive
  2. positive
  3. no effect

1 paper more in this group

See all 5 papers →

co2 · growth · Medicago sativa (alfalfa)Positive and negative results

20 papers: 15 positive, 5 negative or no effect

14 papers in the same direction as this paper · 5 in the opposite direction

  1. negative
  2. negative
  3. no effect

16 papers more in this group

See all 20 papers →

co2 · Aphis craccivora · Medicago sativa (alfalfa)Results agree

2 papers: 0 positive, 2 negative or no effect

1 paper in the same direction as this paper

  1. negative
See all 2 papers →

Claims are grouped by organism, treatment and what was measured or targeted. A paper counts as positive when any of its claims in the group is positive.