Coexistence of mutualist thorn-dwelling ants on camelthorn

acacia in NamibiaHeather Campbell, Mark Fellowes & James

CookSchool of Biological Sciences, University of

Reading @scienceheather

Ant-plant mutualisms • Ant–plant mutualisms widespread (>100

genera of tropical plants & 5/12 ant subfamilies

• Ants defend plants from herbivores & receive food (extrafloral nectar and/or food bodies)

• Myrmecophytes = specialised plants with structures modified for ants, known as domatia

• Single host plant can associate with multiple ant species throughout its lifetime or across geographic range but usually only a single ant species at a time

• Different ant species may vary their provision of antiherbivore defence

Gubb, 1988; Curtis & Mannheimer, 2005

Study site & species

Camelthorn acacia dominated savannah, Kuzikus Wildlife Reserve in Namibian Central Kalahari

• Camelthorn acacia, Vachellia erioloba, is a keystone species & most widespread tree in Namibia

• Under threat from harvesting & land use changes

• Possesses hollow swollen-thorn domatia inhabited by ants, but species & nesting patterns are unidentified

Nest site selection & ant coexistenceWe found four ant species from different genera

Unidentified Crematogaster sp.

Cataulacus intrudens Tapinoma subtile Tetraponera ambigua

Campbell, Fellowes & Cook (In prep.)

In contrast to other African ant plants, many V. erioloba trees (95 % in our survey) were simultaneously co-occupied by multiple ant species

Co-occupancy of myrmecophyte plants by multiple ant species

Provision of antiherbivore defence

• Do domatia characteristics on host plantsa) influence patterns of ant distributions?b) enable/limit ant species coexistence?

• Does each ant species a) provide antiherbivore defence?b) differ in their effectiveness?

Nest site selection & coexistence

Nest site selection & ant coexistence

Cre-mato-gaster

Cataulacus Tapinoma Unoccupied 0

200

400

600

800

1000

1200

1400

1600

1800 a

ab

b

c

Thorn occupant

Dom

atia

vol

ume

(mm

3)

Mean (+ SE) volume (mm3) of swollen-thorn domatia varied significantly with occupant ant species (linear mixed-effects model, Cataulacus n = 40, Crematogaster sp. n = 58, Tapinoma n = 98 and unoccupied n = 135). Letters indicate significant differences (p < 0.01).

Domatia volume differed across thorns occupied by the three ant species and for unoccupied thorns

Campbell, Fellowes & Cook (2013) Insectes Sociaux

Nest site selection & ant coexistence

Cre-mato-

gaster

Cataulacus Tapinoma Unoccupied 0.00

0.20

0.40

0.60

0.80

1.00

1.20

1.40 a

a

b

c

Thorn occupant

Dom

atia

ent

ranc

e ho

le a

rea

(mm

2)

Nest entrance hole size differed between the three ant species occupying thorns and unoccupied thorns

Mean (+ SE) area of entrance hole (mm2) of swollen-thorn domatia varied significantly with occupant ant species (linear mixed-effects model, Cataulacus n = 40, Crematogaster sp. n = 58, Tapinoma n = 98 and unoccupied n = 135). Letters indicate significant differences (p < 0.001).

Campbell, Fellowes & Cook (2013) Insectes Sociaux

2.6 2.8 3.0 3.2 3.4 3.6

0

5

10

15

20

25

Log Volume

Col

ony

size

Log (Domatia volume (mm3))

Squa

re ro

ot (N

umbe

r of a

nts)

Number of ants correlated with species and thorn volume, including interaction in predicting numbers of individuals (also true for proportion of ants that were immatures).

Each species has different nest requirements and different colony response in investment in different life stages.

Nest site selection & ant coexistence

Total number of ant occupants within swollen-thorn domatia were correlated with species identity and thorn volume (ANCOVA, F5, 190 = 41.36, R2 = 0.52, p < 0.00001), as well as interaction term (p < 0.05), resulting in different slopes for each species in predicting the response in numbers of ants to thorn volume; Cataulacus (y = 3.206x-4.658), Crematogaster sp. (y =5.845x-15.247) and Tapinoma (y =12.805x-27.157) Campbell, Fellowes & Cook (2013) Insectes Sociaux

Cataulacus intrudens ___ Crematogaster sp. …

…

Tapinoma subtile ----

Provision of antiherbivore defence by ants

One Two0

5

10

15

20

25

30

35

Trial

Mea

n pe

rcen

tage

of

leafl

ets

dam

aged

per

br

anch

Herbivore damage was higher on branches without ants

Mean (+SE) percentage of leaflets damaged per branch. Black bars are branches with ants experimentally excluded and white bars represent branches with patrolling ants. Campbell, Townsend, Fellowes & Cook (In press) African Journal of Ecology

Provision of antiherbivore defence by antsExplanatory variable Deviance F PColeopteraTreatment 9.75 10.29 <0.01Trial 5.82 6.14 <0.05Treatment x Trial 0.38 0.43 0.5161

HemipteraTreatment 48.43 20.81 <0.0001Trial 20.27 8.71 <0.01Treatment x Trial 0.73 0.31 0.580

LepidopteraTreatment 0.05 0.04 0.84Trial 6.78 5.31 0.03Treatment x Trial 0.01 0.01 0.92

ANODEV table for generalised linear model with quasi-Poisson errors. The minimal adequate model was found by elimination of non-significant terms, beginning from the maximal model. As three separate tests were conducted, we used a Bonferroni-corrected α of 0.0167 to determine significance.Campbell, Townsend, Fellowes & Cook (In press) African Journal of Ecology

The experimental exclusion of ants led to an increase in some insect herbivores, but not lepidopterans.

Provision of antiherbivore defence by ants

No Response Failed eviction Successful eviction0

2

4

6

8

10

12

aab

b

Ant behaviour

Mea

n nu

mbe

r of

ant

s on

bra

nch

Mean (+SE) number of ants present on branch prior to experiment was correlated with response to presence of a G. postica larva (ANOVA, F2,

24=12.2, P<0.001, letters indicate significant differences between groups)

Campbell, Townsend, Fellowes & Cook (In press) African Journal of Ecology

Across all ant species, larvae of G. postica usually ignored (64% of time) Aggressive behaviour only by Crematogaster approx. half of the timeSuccessful eviction correlated with number of ants & tending of scales/treehoppers (P <0.001)

ConclusionMost V. erioloba trees are simultaneously & stably co-occupied by multiple ant species – great opportunity to study coexistence & mutualism

Each ant species occupies nests with different domatia morphology - nest size & availability influences ant colony (different responses in investment in immatures according to availability of nest space)

Presence of ants reduces herbivore damage by some types of insect herbivores but not all (effective against hemipterans and coleopterans, but not lepidopterans)

Only Crematogaster ants show aggression to herbivores but success depends on high numbers of ants & tending of scales/treehoppers

Acknowledgements

Want to know more?

Ministry of Environment and Tourism, Namibia

Field assistants - Gisele Herren & Ian Townsend

Ant identification - Bonnie Blaimer, Brian Taylor, Phil Ward & Peter Hawkes

Email: h.campbell@pgr.reading.ac.ukBlog:

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