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An Australian contribution to the coevolution of red leaf colour hypothesis – courtesy of eucalypts and eucalypt-feeding psyllids

Martin J. Steinbauer & Kevin Farnier

Insect-Plant Interactions Lab, Department of ZoologyLa Trobe UniversityMelbourne, AUSTRALIA

2La Trobe University

Psyllid-eucalypt associations: we have made a start

See poster #97 by Gary Taylor et al.

Psylloidea are basal members of Sternorrhyncha

Extant Psylloidea arose after Angiosperms (Cenozoic; Ouvrard et al.

2010 Syst. Entomol. 35:172-180)

Australian psyllids comprise nearly 380 described spp. in > 50 genera

>50% of spp. use eucalypts; majority are “monophagous”

700+ species in genus Eucalyptus (sens. str.); often co-occur in species-complexes

Utilisation of eucalypts may have preceded utilisation of other hosts

Free-living &lerp-forming spp.

Stem & barkinhabiting spp.


Host selection mechanisms are key component to understanding host specificity

Aphids & whiteflies (Sternorrhyncha) are reliant on vision for host selection

Little known about host selection by Psylloidea

Olfactory sensory neurons of blue gum psyllid sensitive to a range of terpene & green leaf volatiles (Yuvaraj et al. 2012 J. Insect Physiol. 59:542-551) BUT adults of four species do not orientate to host plant odours in Y-tube olfactometer (Farnier & Steinbauer in prep.)

Collapse of white lace lerp psyllid in wild associated with ↑ in total phenolics & ↑ phenolics : amino N ratio (Taylor 1997 Ecology & Evolution of Plant-Feeding Insects in Natural and Man-Made Environments. International Scientific Publications)

Schoonhoven et al. (2005) Insect-Plant Biology. Oxford Uni. Press


Autumnal leaf colouration – phenomenon characteristic of deciduous plants

10 hypotheses relating autumnal colouration to biological factors; inc. protection against abiotic or biotic factors (Archetti 2009 Oikos 118:328-333)

Putative abiotic drivers inc.: Photoprotection

Putative biotic drivers inc.: Unpalatability & Coevolution

Coevolutionary hypothesis: red signals that a plant is not a suitable host for herbivorous insects → preference for green

60c


Autumnal leaf colouration – indicator of leaf senescence

Senescence is final stage of leaf development

Senescence is a controlled process

Visible symptom of senescence is leaf yellowing (chlorosis)

Chlorosis is associated with the mobilisation of proteins & export of sucrose = food for aphids

But aphids must be able to reach chlorotic leaves

Chlorosis can be followed by de novo synthesis of anthocyanins

Holopainen & Peltonen (2002) Oikos 99:184-188Holopainen et al. (2009) Biol. Letters 5:603-605


Nymphs of some eucalypt-feeding psyllids induce premature senescence of old (expanded) leaves

a: early instar Cardiaspina nymphs on Grey box leaf in October 2012 → chlorotic lesions just visible below lerps

b: late instar Cardiaspina nymphs + empty lerps on Grey box leaf in November 2012 → chlorotic lesions spread into tissues surrounding lerps and coalasced

Steinbauer et al. (under revision) Oecologia


Feeding-induced chlorosis is associated with nutritional enhancement of leaves

Chlorophyll reduced by v high #s of nymphs

Concentrations of all FAAs increased by nymphs

Essential FAAs elevated by v high #s of nymphs

(Phenols not measured for this study)

total chlorophyll (microgram

per mg leaf)

0.6

0.8

1.0

1.2

1.4

1.6

1.8

2.0

2.2

all amino acids &

amine m

etabolites(nanom

oles per mg leaf)

1

2

3

4

5

6

7

8

9

10

11

12

13

14

October November

essential amino acids (%

)

7

8

9

10

11

12

13

14

15

16

17

(a)

(b)

All amino acids

Essential amino acids

Chlorophyll

October November

V HIGH #s

HIGH #s

ZEROV HIGH #s

HIGH #s

ZERO

ZERO

V HIGH #s

HIGH #s

**

0.087

**

***

***

n.s.

n.s.



Nutritional enhancement of host leaves beneficial to nymphs

Intra-specific competition reduces individual access to nutrients

Adults may feed around lesions caused by nymphs


HIGH V HIGH

forewing pad length (m

m)

0.20

0.22

0.24

0.26

0.28

0.30

0.32

*

IV instar nymphs

HIGH V HIGH


m)

0.50

0.55

0.60

0.65

0.70

0.75

0.80

0.85

*

V instar nymphs

HIGH V HIGH


m)

0.64

0.66

0.68

0.70

0.72

0.74

0.76

0.78

0.80

0.82

0.84

V instar FEMALE nymphs

***


Chlorosis can be a prelude to anthocyanin synthesis – red leaves symptom of cold-induced photoinhibition

Steinbauer et al. (in prep.)

Anthocyanic lesions around abandoned psyllid lerps are evident in Austral spring

Enzymes from feeding nymphs delay anthocyanin synthesis

Close et al. (2003) Ecology 84:2952-2966


Psyllid feeding in spring associated with higher concentrations of anthocyanins but red leaves not necessarily higher in phenolics


(Free amino acid data unavailable prior to SIP 15)

number of psyllids per leaf

0 50 100 150 200 250

anthocyanin concentration (microgram

s per mL)

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

1.8

anthocyanin concentration (micrograms per mL)

0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8total phenolics concentration (gallic acid equivalents

microgram

s per mL)

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

red leaves (psyllid infested during spring)green leaves (psyllid infested during summer)

anthocyanin concentration (micrograms per mL)

0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8

total phenolics concentration

(gallic acid e

quivalen

tsm

icrograms per m

L)

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

red leaves (psyllid infested during spring)green leaves (psyllid infested during summer)


Anthocyanin synthesis is a brief prelude to leaf necrosis


Anthocyanic lesions arising from feeding damage typically die within one month of nymphs vacating lerps

Undamaged tissues remain green

This leaf became noticeably less green in February and was abscised before March photo

October 2013

January 2014

% o

f lea

f are

a

chlorotic

anthocyanic

necrotic


BUT WHAT ABOUT YOUNG EUCALYPT LEAVES?

Young (expanding) leaves of many species of eucalypt are red

High foliar anthocyanin expression linked to low photosynthetic capacity

Anthocyanins provide photoprotection before critical chlorophyll concentration accumulated (Close & Beadle 2003 Bot. Rev. 69:149-161)

Concentrations of total phenolics (& other PSMs) are typically low in very young leaves but rise to a peak at around 200 days (McArthur et al. 2010 Austr. Ecol. 35:157-166)


Quantifying visual sensitivities of psyllids

Stimuli tested first are colours printed onto card (above right)

Leaf sections sandwiched between glass coverslips using silicone grease tested subsequently; permits control of olfactory confound (bottom right)

Farnier et al. (under revision) Front. Ecol. Evol.


Some psyllids specialised on expanding eucalypt leaves also exhibit attraction to “red”

2/4 species have exhibited red preference

Red preference is independent of stimulus intensity

UV-blue-green model (as for aphids) does not satisfactorily explain red attraction

1/2 species exhibits strong visual attraction to young “red” leaves

Farnier et al. (under revision) Front. Ecol. Evol.Farnier et al. (in prep.)

Card bioassays

Anoeconeossabundoorensis

Glycaspisbrimblecombei

Sandwiched leaf section bioassays


SUMMARY: psyllid specialisation on expanded eucalypt leaves

Temporal production of photoinhibited leaves brief and not coincident with host searching adults

Anthocyanin accumulation in feeding-damaged leaves not directly linked to nutritional enhancement AND anthocyanic tissues about to die

Senescence leaf colour probably exerts negligible selective pressure

Senescence-inducing feeding strategy is successful, e.g. Cardiaspina comprises 24 described spp.

We do not expect a high incidence of red perception in these species

October 2013

December 2013


SUMMARY: psyllid specialisation on expanding eucalypt leaves

Temporal production of young leaves protracted and coincident with host searching adults

Leaf colour likely to provide honest indicator of nutritional quality since linked to the host plant’s physiology

Expanding leaf colour probably exerts strong selective pressure

Glycaspis comprises 137 described spp.

Anoeconeossa comprises 17 described spp.

We expect a higher incidence of red perception in these speciesEyes of Glycaspis brimblecombei courtesy of

(a) Rita Wallén & (b) Carina Rasmussen of Vision Group, Lund University

Thank you

latrobe.edu.au CRICOS Provider 00115M

Funding: ARC Future Fellowships (MJS)

Australia & Pacific Science Foundation (MJS)Australian Postgraduate Award (KF)

Assistance: Gary Taylor (UAdel); Mike Dann, Anna Burns, Beryn Otieno, Richard Peters, Simon Watson (LTU); Adrian Dyer (RMIT); Aidan Hall, Markus Riegler (UWS); Dugald Close (UTas); Berin Boughton, Ute Roessner (UMelb); Andrew Merchant (USyd); Eric Warrant, Almut Kelber (Lund University)

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