The golden mimicry complex uses a wide spectrum of defence to deter a community of predators
- Masaryk University, Czech Republic
- Macquarie University, Australia
Figures
Figure 1
Projection of the mimicry complex on a pruned phylogenetic tree.
The tips of the tree represent species and full circles are coloured according to putative ring classification. Representatives of each ring are shown. Four types of defence are projected on the branches.
Figure 2
Modes of production of the golden shine.
(A) Polyrhachis ammon, gaster, SEM. (B) P. ammon, detail of hairs. (C) Dolichoderus clarki, gaster, SEM. (D) D. clarki, detail of hairs. (E) Myrmecia tepperi, gaster, SEM. (F) M. tepperi, detail of hairs. (G) Camponotus aeneopilosus, gaster, SEM. (H) C. aeneopilosus, detail of hairs. (I) Ephutomorpha aurata, gaster, SEM. (J) E. aurata, detail of hairs. (K) Daerlac nigricans, gaster, SEM. (L) D. nigricans, pigment. (M) Myrmarachne luctuosa, abdomen, SEM. (N) M. luctuosa, pigment on abdomen. (O) Eurymela rubrolimbata, pigment on gaster. SEM (A–K, M) and light photography (L, N, O) of the dorsal side of mimics.
Figure 3
Mimetic rings and their distribution.
(A) NMDS ordination of species classified into ten putative rings (stress = 0.16). The rings were distinguished by k-means clustering using ssi criterion (in which the maximum value indicates the correct number of clusters), which is shown on the right of the plot. (B) Map of distribution of ten putative rings in Australia.
Figure 4
Effect of unpalatability.
(A) Histogram of unpalatability of the mimetic complex with horizontal boxplots for each ring. (B) Relationship between the absolute area of dorsal golden colouration of mimics and their unpalatability. (C) Relationship between unpalatability and post-attack response of skinks to the six prey species from being eaten (0), to cleaning its mouth (0.5) and spitting out the prey item (1).
Figure 5
Relationship between unpalatability and predation pressure.
(A) Relationship between unpalatability and the total predation pressure (K-value) on 13 mimics by three guilds of predators (visually-oriented euryphagous, specialized ant-eating, non-visually-oriented ant-adverse). Estimated non-parametric regression model (GAM) is displayed. See Table 2 for unpalatability of mimics. (B) Relationship between unpalatability of five mimics and total predation pressure (K-value) from three representatives of predators (see Table 3 for unpalatability of mimics). A high K-value indicates high predation while a low K-value indicates low predation. Solid symbols = Batesian mimics, hollow symbols = Müllerian mimics.
Figure 6
Capture of mimics by three predators.
Comparison of frequency of attacks on five mimics and one non-mimic by skinks (euryphagous visually-oriented predator); Lampona spiders (ant-adverse non-visually oriented predators), and Servaea spiders (specialised ant-eating predators).
Figure 7
Selected list of 100 species representing the ten putative mimetic rings.
Species are arranged within each ring from the most to the least unpalatable (left to right). Some pictures of ants are displayed with the permission of AntWiki and R. Kohout.
Figure 8
Relationship between cuticle thickness and thorax length.
(A) poison/pygidial gland area and gaster length (B) sting length and gaster length (C) with estimated linear regression models.
Videos
Video 1
Overview of selected mimetic species belonging to the golden complex.
https://doi.org/10.7554/eLife.22089.005Tables
Table 1
List of mimic species belonging to the golden complex arranged according to the order, family (subfamily), and genus (subgenus).
Order | Family (Subfamily) | Genus (Subgenus) | Species |
|---|---|---|---|
Hymenoptera | Formicidae (Formicinae) | Camponotus | aeneopilosus Mayr; aurocinctus (Smith); bigenus Santschi; ephippium (Smith); fergusoni McArthur; nigroaeneus (Smith); oxleyi Forel; piliventris (Smith); setosus Shattuck and McArthur; suffusus (Smith); tasmani Forel; thadeus Shattuck; wiederkehri Forel |
|
| Polyrhachis (Chariomyrma) | appendiculata Emery; arcuata (Le Guillou); aurea Mayr; bedoti Forel; constricta Emery; cydista Kohout; cyrus Forel; guerini Roger; heinlethii Forel; lata Emery; obtusa Emery; pallescens Mayr; schoopae Forel; senilis Forel; vermiculosa Mayr |
|
| Polyrhachis (Hagiomyrma) | ammon (Fabricius); ammonoeides Roger; anderseni Kohout; angusta Forel; archeri Kohout; aurora Kohout; brisbanensis Kohout; brutella Kohout; burwelli Kohout; callima Kohout; capeyorkensis Kohout; conciliata Kohout; cracenta Kohout; crawleyi Forel; darlingtoni Kohout; denticulata Karavaiev; diversa Kohout; dougcooki Kohout; electra Kohout; elengatula Kohout; feehani Kohout; hoffmani Kohout; melanura Kohout; nourlangie Kohout; penelope Forel; pilbara Kohout; placida Kohout; seducta Kohout; semiaurata Mayr; stricta Kohout; tanami Kohout; tenebra Kohout; thusnelda Forel; trapezoidea Mayr; tubifera Forel; unicaria Kohout; vernoni Kohout; weiri Kohout |
|
| Polyrhachis (Hedomyrma)
| argentosa Forel; barretti Clark; cleopatra Forel; consimilis Smith; cupreata Emery; daemeli Mayr; erato Forel; euterpe Forel; hermione Emery; mjobergi Forel; ornata Mayr; rufifemur Forel; terpsichore Forel; thais Forel |
| Formicidae (Formicinae) | Polyrhachis (Myrma) | andromache Roger; foreli Kohout; inusitata Kohout
|
|
| Polyrhachis (Myrmhopla) | dispar Kohout; dives Smith; reclinata Emery; sexspinosa (Latreille) |
|
| Polyrhachis (Polyrhachis) | bellicosa Smith |
| Formicidae (Dolichoderinae) | Dolichoderus | angusticornis Clark; clarki Wheeler; dentatus Forel; doriae Emery; extensispinus Forel; inferus Shattuck and Marsden; niger Crawley; rufotibialis Clark; scabridus Roger; scrobiculatus (Mayr); turneri Forel |
|
| Iridomyrmex | anderseni Shattuck; azureus Viehmeyer; coeruleus Heterick and Shattuck; roseatus Heterick and Shattuck; ypsilon Forel |
| Formicidae (Myrmeciinae) | Myrmecia | athertonensis Forel; auriventris Mayr; borealis Ogata and Taylor; chrysogaster (Clark); cydista (Clark); eungellensis Ogata and Taylor; fabricii Ogata and Taylor; flavicoma Roger; fulviculis Forel; fulvipes Roger; gilberti Forel; harderi Forel; luteiforceps Wheeler; mandibularis Smith; michaelseni Forel; petiolata Emery; piliventris Smith; rugosa Wheeler; tepperi Emery; tridentata Ogata and Taylor |
| Formicidae | Diacamma | schoedli Shattuck and Barnett |
| (Ponerinae) | Pachycondyla | sublaevis (Emery) |
| Mutillidae | Ephutomorpha | aurata (Fabricius) |
Hemiptera | Eurymelidae | Eurymela | rubrolimbata Kirkaldy |
| Rhyparochromidae | Daerlac | apicalis (Distant); cephalotes (Dallas); nigricans Distant |
Araneae | Salticidae | Myrmarachne | erythrocephala forma erato (L. Koch); erythrocephala forma ornata (L. Koch); erythrocephala forma daemeli (L. Koch); luctuosa forma aeneopilosa (L. Koch); luctuosa forma aurea (Ceccarelli); macleayana forma foreli (Bradley) |
|
| Ligonipes | illustris Karsch |
|
| Ohilimia | scutellata (Kritscher) |
| Corinnidae | Nyssus | luteofinis Raven |
| Gnaphosidae | Eilica | sp. |
Table 2
The percentage of predator individuals found with DNA (Next Generation Sequencing) of mimics in their gut/faeces. The primer specific for ants amplified on average 9.3% individuals of predators, the primer specific for Myrmarachne spiders amplified 3.9% individuals of predators, and the primer specific for mutillids amplified 9.2% individuals of predators. The predators (553 spiders, 50 skinks, 48 birds) were collected on the Macquarie University campus. They are grouped according to their guild. N gives the number of individual predators screened. The mimics are arranged from the most to the least palatable (left to right).
Predatory guild Species (Family) | P. ornata | P. vermiculosa | P. aurea | P. ammon | P. erato | M. piliventris | M. tepperi | C. aeneopilosus | E. aurata | D. cephalotes | D. nigricans | M. erythrocephala | M. luctuosa | N |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Visually-oriented euryphagous | ||||||||||||||
Eulamprus quoyii (Scincidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 50 |
Manorina melanocephala (Meliphagidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0.02 | 0 | 0 | 0 | 0.04 | 0 | 48 |
Sandalodes superbus (Salticidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 37 |
Holoplatys planissima (Salticidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 12 |
Ocrisiona sp. (Salticidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 3.8 | 3.8 | 26 |
Specialised ant-eating | ||||||||||||||
Servaea incana (Salticidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1.8 | 114 |
Euryopis umbilicata (Theridiidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 9.9 | 8.6 | 101 |
Euryopis sp. (Theridiidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 12 |
Hemicloea sp. 1 (Gnaphosidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 5.0 | 0 | 0 | 0 | 0 | 0 | 20 |
Hemicloea sp. 2 (Gnaphosidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 2.4 | 0 | 0 | 0 | 2.4 | 2.4 | 42 |
Non-visually oriented euryphagous | ||||||||||||||
Lampona murina (Lamponidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 2.2 | 4.3 | 46 |
Clubionia robusta (Clubionidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1.7 | 58 |
Clubiona sp. (Clubionidae) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 2.4 | 2.4 | 85 |
Table 3
A list of traits used to assess the unpalatability of five mimics. Values are means (±SE) estimated from 10 measurements. The species are arranged from the most to the least palatable.
Species | Frequency of biting | Spray chemicals | Number of spines | Total spines length [mm] | Cuticle thickness [mm] | Total body size [mm] | Mandible size [mm] | Gland size [mm2] |
|---|---|---|---|---|---|---|---|---|
P. ammon | 0.1 | 1 | 4 | 3.54 (0.08) | 0.04 (0.002) | 9.04 (0.08) | 1.00 (0.02) | 2.84 (0.16) |
P. vermiculosa | 0 | 1 | 6 | 2.96 (0.08) | 0.03 (0.002) | 5.98 (0.05) | 0.71 (0.03) | 1.62 (0.06) |
C. aeneopilosus | 0.3 | 1 | 0 | 0 | 0.02 (0.001) | 8.04 (0.17) | 0.84 (0.02) | 2.43 (0.09) |
D. nigricans | 0 | 0 | 0 | 0 | 0.02 (0.0002) | 7.40 (0.14) | 0 | 0.57 (0.03) |
M. luctuosa | 0 | 0 | 0 | 0 | 0.02 (0.001) | 7.04 (0.28) | 0 | 0 |
Table 4
List of primer pairs used to identify mimics in the gut or faeces of potential predators.
Primer | Sequence | Fragment length (bp) | Amplified genera |
|---|---|---|---|
DaerF | 5´- GAT CAA ATT TAT AAT AC −3´ | 204 | Daerlac |
DaerR | 5´- TTC TGA TTA ATA AGG −3´ | ||
FormF | 5´- GAT CAA ACY TTT AAY TC −3´ | 220 | Camponotus, Myrmecia, Polyrhachis |
FormR | 5´- CCW GAT CCT TCA TTA ATA AA −3´ | ||
MyrmF | 5´- ATT AGC TTC TAT TAT TG −3´ | 142 | Myrmarachne |
MyrmR | 5´- TCT ATA GAA ATW CCT TCA G −3´ | ||
BothmF | 5´- TCC TCA TGT TCA GGA ATA ATT AA −3´ | 215 | Bothriomutilla |
BothmR | 5´- ATT AAG AGC ATA ATG GAT ATT GGG −3´ |
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The golden mimicry complex uses a wide spectrum of defence to deter a community of predators
eLife 6:e22089.
https://doi.org/10.7554/eLife.22089
