Fukatsu, Takema

Katayama, Noboru

Kutsukake, Mayako

Meng, Xian-Ying

Nikoh, Naruo

Shibao, Harunobu

English

Sydney eScholarship

How do gall-forming social aphids keep their closed nest clean?	Mayako Kutsukake1, Xian-Ying Meng1, Noboru Katayama2, Naruo Nikoh3, Harunobu Shibao4 & Takema Fukatsu1 1AIST, Japan, 2Kyoto University, Japan, 3The Open University of Japan, Japan, 4University of Tokyo, Japan, e-mail: m-kutsukake@aist.go.jp P129	Reference: Kutsukake M., Meng X-Y., Katayama N., Nikoh N, Shibao H. and Fukatsu T. (2012) An insect-induced novel plant phenotype for sustaining social life in a closed system. Nat. Commun. 3: 1187�Introduction: waste problems in aphid galls	Soldiers discard honeydew droplets from gall openings. Open galls� 1 cm	Soldier �honeydew �Openings �l  No accumulation of honeydew were detected in closed galls of N. monzeni. l  However, N. monzeni aphids produced honeydew on an artificial diet system. 1 mm	0.5 mm	Hypothesis Is the honeydew absorbed by the gall tissue? Adult �Soldier  nymph�Powdery wax �Gall inside �Honeydew droplets �(Ⅰ) Field experiments Water-absorbing property in completely closed galls of N. monzeni (1)  Bored a small hole  (2)  Injected 1ml of water or sucrose solution (3) Sealed the hole with an adhesive �Amount of the solution remained in the gall after 20 h were measured. �Results �Methods �Gall�(Ⅲ) Where was the water ������ transported? (Ⅱ) Sugar analysis of aphid       honeydew Artificial diet�In	Spongy wax layer	Cell wall	Plant cell	1 µm	1 cm	Water-absorbing closed gall Aphid: N. monzeni Host plant:  Distylium racemosum	Gall inner surface after placing a drop of water  Transmission electron microscopy  of the gall inner surface  00.2 0.4 0.6 0.8 1.0 35 34 5 10 11 14 25 12 25 7 11 14 19 44 50 41 Volume of absorbed solution (ml) DW (N=16)�-0.2 0 0.2 0.4 0.6 0.8 1.0 -0.4 23 11 9 16 10 62 9 23 12 8 21 60 37 0 0.2 0.4 0.6 0.8 1.0 19 61 21 16 66 2% sucrose � 4% sucrose � 8% sucrose (N=6 each)�Gall  volume (ml) 15 of 16 galls absorbed water completely! The lower sugar concentration,  the easier the solution to be absorbed.  Results �Methods: HPLC�0 50 100 150 200 250 300 350 400 450 500 (mM) N. monzeni < 0.5% Fructose �Glucose �Sucrose �Trehalose �Melezitose �Sugar concentration of N. monzeni honeydew was low enough to be absorbed by the gall tissue. Results �Methods: Water absorption routes was stained by 0.5ml of 0.2% safranin solution for 20 h.�Out �In� 0.2 mm	1 cm	Inside view of a safranin-absorbed gall The safranin solution  was absorbed from here Histological section of the stained gall  Vein-like staining	Vascular bundle	The absorbed water was removed by the vascular bundle system. Why watery waste is absorbed by closed galls, but not by open galls? We observed closed galls, but surprisingly, 1 cm	Soldiers can NOT remove honeydew Closed galls A gall of Nipponaphis monzeni�No openings	in	1 cm	Water-unabsorbing open gall Aphid: T. styraci Host plant:  Styrax obassia	Hydrophobicity and ultrastructure of inner surface of closed and open galls were examined. Water-absorbing closed gall Aphid:  Ceratovacuna nekoashi Host plant:  Styrax japonicus	Water-unabsorbing open gall Aphid: Ceratovacuna japonica Host plant:  Styrax japonicus	Hydrophilic inner surface	Hydrophobic inner surface	Thin and spongy  surface layer	Thick and distinct  wax layer	Two congenic aphid galls on the same plant	 Gall inner surface after placing a drop of water  Transmission electron microscopy  of the gall inner surface In	Thick wax layer	Cell wall	Plant cell	1 µm	Hydrophilic inner surface	Hydrophobic inner surface	Thin and spongy  surface layer	Thick and distinct  wax layer	 1 µm	1 µm	Spongy wax layer	Cell wall	Cell wall	Thick wax layer	Cell wall	Structural differences of the wax layer of the gall inner surface determined the water-absorbing property. The aphids, but not the plants, induced the water-absorbing property by manipulation of gall morphology and physiology. Conclusion	Closed gall-forming aphids induced a plant-mediated waste removal system to reconcile colony defense and hygiene,  which can be regarded as “indirect social behavior” of the social aphids.	A gall of Tuberaphis styraci�Plant sap-sucking aphids produce sticky honeydew, which drowns and kills aphids if it accumulates in the gall. 	Summary	Some social aphids form completely closed galls on their host plants, wherein hundreds to thousands of aphids grow and reproduce for at least a several months in isolation. So far, why the aphids in closed galls are not drowned and killed by accumulated honeydew has been an enigma. In this study, we	found a novel plant phenotype that the inner wall of the closed galls absorbed and removed honeydew via the vascular bundle system. This plant-mediated waste removal system was induced by aphids, but not by plants, due to their manipulation of gall morphology and physiology, which could be regarded as “indirect social behavior” of the social aphids.	In	In	

How do gall-forming social aphids keep their closed nest clean?

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How do gall-forming social aphids keep their closed nest clean?

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