Arthropod Natural Products as Insect Repellents - American Chemical

Chapter 2

Arthropod Natural Products as Insect Repellents Murray S. Blum , Daniel M. Everett , Tappey H. Jones , and Henry M. Fales 1

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Department of Entomology and Department of Computer Science, University of Georgia, Athens, GA 30602 Laboratory of Chemistry, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892

Downloaded by UNIV OF TEXAS EL PASO on August 20, 2014 | http://pubs.acs.org Publication Date: January 9, 1991 | doi: 10.1021/bk-1991-0449.ch002

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The defensive allomones of arthropods have been evolved to blunt the attacks of a variety of predatory species. These natural products function primarily by repelling adversaries and thus usually constitute the first line of defense. An examination of the deterrent efficacies of compounds produced by honey bees, thrips, and ants demonstrates that these exocrine products are highly effective repellents against a diversity of ant species. A potpourri of natural products including aliphatic and aromatic ketones, esters, fatty acids, and alkaloids has been determined to possess well-developed repellent properties at physiological concentrations. These results emphasize the great potential of insect-derived compounds as an outstanding source of repellents in the never-ending battle with species of pest arthropods.

Among a n i m a l s , a r t h r o p o d s a r e d i s t i n g u i s h e d by t h e i r u t t e r dominance i n terms o f b o t h numbers o f s p e c i e s and i n d i v i d u a l s . The v i r t u a l u b i q u i t y o f t h e s e populous organisms guarantees t h a t t h e y w i l l be s u b j e c t t o g r e a t p r e d a t o r y p r e s s u r e from t h e i n v e r t e b r a t e s and v e r t e b r a t e s w i t h which t h e y s h a r e t h e i r f r a g i l e w o r l d . N o t s u r p r i s i n g l y , a r t h r o p o d s themselves c o n s t i t u t e a major group o f p r e d a t o r s , and among t h e s e , i t i s n o t u n l i k e l y t h a t a n t s a r e dominant. Indeed, a n t s a r e p r o b a b l y t h e major p r e d a t o r y a n i m a l s i n t h e w o r l d , w i t h most o f t h e i r 10,000-15,000 s p e c i e s (1) e x h i b i t i n g a c a r n i v o r o u s p r o p e n s i t y combined w i t h an e f f i c i e n t system o f p r e y a c q u i s i t i o n ( 2 ) . F o r most a r t h r o p o d s , a n t s p r o b a b l y r e p r e s e n t t h e most f r e q u e n t l y encountered p r e d a t o r s w i t h which t h e y must contend. Defense a g a i n s t a n t s and t h e l e g i o n s o f o t h e r p r e d a t o r y a n i m a l s thus becomes a s i n e qua non f o r t h e s u r v i v a l o f a r t h r o p o d o u s species i n a v a r i e t y of ecological contexts. 0097-6156/91/0449-0014$06.00/0 © 1991 American Chemical Society In Naturally Occurring Pest Bioregulators; Hedin, P.; ACS Symposium Series; American Chemical Society: Washington, DC, 1991.


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B L U M ET AL.

Arthropod Natural Products as Insect Repellents

A r t h r o p o d s s y n t h e s i z e an i n c r e d i b l e d i v e r s i t y o f n a t u r a l p r o d u c t s i n t h e i r e x o c r i n e g l a n d s (3) w h i c h a r e u t i l i z e d w i t h g r e a t e f f e c t i v e n e s s t o b l u n t t h e a t t a c k s of t h e i r a d v e r s a r i e s . The d e f e n s i v e s e c r e t i o n s o f t h e s e i n v e r t e b r a t e s can o f t e n be d e l i v e r e d w i t h great accuracy, thus ensuring t h a t aggressive p r e d a t o r s a r e s u b j e c t e d t o t h e f u l l impact o f t h e s e s e c r e t o r y e f f r o n t e r i e s ( 4 ) . S i g n i f i c a n t l y , t h e s e exudates u s u a l l y m a n i f e s t t h e i r d e f e n s i v e e f f i c a c y as e f f e c t i v e r e p e l l e n t s and t h u s c o n s t i t u t e the f i r s t l i n e o f defense o f t h e p r e y s p e c i e s . The d e t e r r e n t v a l u e o f t h e n a t u r a l p r o d u c t s i n t h e s e s e c r e t i o n s i s i n e s t i m a b l e , s i n c e i t can p e r m i t t h e i r p r o d u c e r s t o escape predators without i n j u r i o u s p h y s i c a l confrontations. This i s e s p e c i a l l y important i n encounters w i t h ants, s i n c e these s o c i a l i n s e c t s can q u i c k l y l a u n c h d e v a s t a t i n g en masse a t t a c k s . A v a r i e t y o f s t u d i e s has demonstrated t h a t a n t s may be r a p i d l y d e t e r r e d by t h e d e f e n s i v e s e c r e t i o n s of d i v e r s e a r t h r o p o d s on w h i c h t h e y attempt t o p r e y ( 5 , 6 ) . For example, many o f t h e s m a l l and d e l i c a t e s p e c i e s o f t h r i p s ( T h y s a n o p t e r a ) produce a n a l s e c r e t i o n s t h a t a r e d i r e c t e d a g a i n s t t h e a n t s w i t h w h i c h t h e y f r e q u e n t l y have e n c o u n t e r s (7). Although the d e f e n s i v e s e c r e t i o n s o f v e r y few t h r i p s s p e c i e s have been a n a l y z e d , e v a l u a t i o n o f t h e compounds p r e s e n t i n a few o f t h e s e exudates i n d i c a t e s t h a t t h e y a r e e f f e c t i v e d e t e r r e n t s f o r a n t s ( 8 , 9 ) . These r e s u l t s f u r t h e r suggest t h a t r e p e l l e n t s f o r a n t s may be commonly e n c o u n t e r e d i n t h e d e f e n s i v e s e c r e t i o n s o f a v a r i e t y o f a r t h r o p o d o u s s p e c i e s . F u r t h e r m o r e , s i n c e a n t s have frequent a n t a g o n i s t i c i n t e r a c t i o n s w i t h other species of ants, i t c o u l d be a n t i c i p a t e d a p r i o r i t h a t t h e s e f o r m i c i d s would have e v o l v e d p o w e r f u l ant d e t e r r e n t s t h e m s e l v e s . B o t h f i e l d and l a b o r a t o r y s t u d i e s have documented t h e d e t e r r e n t e f f i c a c i e s t o a n t s o f the venomous s e c r e t i o n s o f t h e s e i n s e c t s (10, Γ1, _12). For example, i t has been demonstrated t h a t t h e r a i d i n g modus v i v e n d i of one ant s p e c i e s was made p o s s i b l e by the u t i l i z a t i o n of a venom-derived a l k a l o i d t h a t i s a p o w e r f u l r e p e l l e n t f o r workers o f r a i d e d ant s p e c i e s ( 1 3 ) . A l t h o u g h a n t s s y n t h e s i z e an i n c r e d i b l e d i v e r s i t y o f venomous a l k a l o i d s ( 1 4 ) , t h e i r a c t i v i t i e s as r e p e l l e n t s f o r t h e s e f o r m i c i d s have o n l y been d e s c r i b e d p r e l i m i n a r i l y ( 1 5 ) . S i g n i f i c a n t l y , a n t s appear t o be t y p i c a l o f s o c i a l i n s e c t s i n g e n e r a t i n g d e t e r r e n t compounds i n t h e i r e x o c r i n e g l a n d s , and examples of o t h e r hymenopterans p r o d u c i n g r e p e l l e n t s , o f g r e a t s o c i a l s i g n i f i c a n c e , have r e c e n t l y been r e p o r t e d ( 1 6 ) . Honey bee queens produce a r e c t a l s e c r e t i o n w h i c h r e p e l s a g g r e s s i v e workers i n t h e c o l o n y as an example o f an i n t r a s p e c i f i c r e p e l l e n t ( 1 6 ) . I f such pheromonal r e p e l l e n t s a r e commonly produced by s o c i a l i n s e c t s , a c o r n u c o p i a o f d e t e r r e n t n a t u r a l p r o d u c t s a w a i t s i d e n t i f i c a t i o n i n the exocrine s e c r e t i o n s of these arthropods. I n the p r e s e n t r e p o r t , we p r e s e n t r e s u l t s o f v e r y r e c e n t i n v e s t i g a t i o n s on t h e c h e m i s t r y and d e t e r r e n t a c t i v i t i e s t o a n t s o f the d i v e r s e compounds i d e n t i f i e d as e x o c r i n e compounds o f t h r i p s . I n a d d i t i o n , we e v a l u a t e the r e p e l l e n c y o f some honey bee n a t u r a l p r o d u c t s t o honey bee workers as an example o f how pheromones themselves can be c a n d i d a t e s as d e t e r r e n t s

In Naturally Occurring Pest Bioregulators; Hedin, P.; ACS Symposium Series; American Chemical Society: Washington, DC, 1991.

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NATURALLY OCCURRING PEST BIOREGULATORS

f o r t h e s p e c i e s t h a t produce them. F i n a l l y , d e t a i l e d a n a l y s e s o f the r e p e l l e n c i e s of a host of n i t r o g e n h e t e r o c y c l e s i d e n t i f i e d i n t h e venoms o f a n t s a r e d e s c r i b e d .


C h e m i s t r y and R e p e l l e n c y o f T h r i p s N a t u r a l

Products

The f i r s t compound i d e n t i f i e d as a n a t u r a l p r o d u c t o f t h r i p s was V - d e c a l a c t o n e ( I ) , a p r o d u c t o f B a g n a l l i e l l a yuccae ( 8 ) . The a n a l e x u d a t e , w h i c h i s d i s c h a r g e d when t h e t h r i p s a r e d i s t u r b e d , does not c o n t a i n any o t h e r d e t e c t a b l e v o l a t i l e s . B o t h l a b o r a t o r y and f i e l d s t u d i e s demonstrated t h a t t h e s e c r e t i o n e f f e c t i v e l y d e t e r r e d a n t w o r k e r s e i t h e r as a t o p i c a l i r r i t a n t o r by r e p e l l e n c y p e r s e . Workers o f Monomorium minimum q u i c k l y withdrew a f t e r c o n t a c t w i t h t h e a n a l f l u i d and a v o i d e d s i t e s a t w h i c h t h e exudate had been r e l e a s e d ( 8 ) . The r e p e l l e n c y o f t h e a n a l exudate was c l e a r l y i d e n t i f i e d w i t h T - d e c a l a c t o n e , two t h r i p s e q u i v a l e n t o f t h i s compound e v o k i n g 50% r e p e l l e n c y f o r minimum w o r k e r s . S i m i l a r r e s u l t s were o b t a i n e d w i t h p h a r a o n i s and h u m i l i s , two o t h e r s p e c i e s o f p r e d a t o r y a n t s . The r e s u l t s o f f i e l d s t u d i e s corroborated the laboratory findings ( 8 ) .

7-Decalactone

The c h e m i s t r y and r e p e l l e n t e f f i c a c y o f t h e a n a l exudate o f t h e Cuban l a u r e l t h r i p s , G y n a i k o t h r i p s f i c o r u m , a g a l l - i n h a b i t i n g s p e c i e s , have a l s o been examined ( 9 ) . The exudate i s dominated by a 1:1 r a t i o o f h e x a d e c y l a c e t a t e and pentadecane; t e t r a d e c y l a c e t a t e , t r i d e c a n e , t e t r a d e c a n e , and heptadecane c o n s t i t u t e minor concomitants. The a n a l s e c r e t i o n o f Gj_ f i c o r u m i s b o t h an e f f e c t i v e c o n t a c t d e t e r r e n t and r e p e l l e n t f o r a g g r e s s i v e a n t s . Workers o f Wasmannia a u r o p u n c t a t a a r e r a p i d l y r e p e l l e d by an a n a l d r o p l e t from a t h r i p s t h a t i s w i t h i n a m i l l i m e t e r o f t h e a n t s (9). T o p i c a l t r e a t m e n t o f a n t s w i t h a n a l exudate c o r r e s p o n d i n g t o 0.25 t h r i p s e q u i v a l e n t s r e s u l t e d i n 100% o f t h e workers d r a g g i n g t h e m s e l v e s away from t h e scene o f t h e encounter i n much t h e same manner as o c c u r s when t h e s e a n t s c o n t a c t t h e t h r i p s under f i e l d c o n d i t i o n s . B o t h h e x a d e c y l a c e t a t e and pentadecane caused dragging behavior a f t e r being a p p l i e d t o ant workers, which responded i n a dose-dependent manner. S i g n i f i c a n t l y , a l t h o u g h h e x a d e c y l a c e t a t e i s more a c t i v e than pentadecane, a c o m b i n a t i o n o f t h e two compounds i s c o n s i d e r a b l y more e f f e c t i v e t h a n t h e e q u i v a l e n t amounts o f e i t h e r o f t h e two compounds a l o n e . T h e r e f o r e , i t i s e v i d e n t t h a t t h e e s t e r and h y d r o c a r b o n i n t e r a c t



2. B L U M ET A L


s y n e r g i s t i c a l l y t o augment t h e d e t e r r e n t e f f i c a c y o f t h e exudate (2). R e c e n t l y , t h e c h e m i s t r y o f t o t a l e x t r a c t s o f another s p e c i e s o f G y n a i k o t h r i p s was examined ( Γ7 ). G. u z e l i i s r e p o r t e d t o produce t h e same h y d r o c a r b o n s and a c e t a t e s as G. f i c o r u m , b u t i n a d d i t i o n s y n t h e s i z e s a n o v e l monoterpene, β-acaridial, a compound r e c e n t l y i d e n t i f i e d as a n a t u r a l p r o d u c t o f a m i t e (18). βA c a r i d i a l has a l s o been i d e n t i f i e d as an i m p o r t a n t compound produced by two o t h e r s p e c i e s o f t h r i p s , V a r s h n e y i a p a s a n i i and L i o t h r i p s kuwanai (Γ7). The f u n c t i o n o f β-acaridial, w h i c h i s v e r y u n s t a b l e , i s n o t known. Another monoterpene, p e r i l l e n e , has been i d e n t i f i e d as a p r o d u c t o f t h r i p s i n s e v e r a l genera. T h i s furanomonoterpene accompanies β-acaridial i n e x t r a c t s o f V. p a s a n i i , L. kuwanai, and L. p i p e r i n u s (19, 2 0 ) . P e r i l l e n e has a l s o been d e t e c t e d as a major p r o d u c t i n e x t r a c t s o f T e u c h o t h r i p s l o n g u s , A r r h e n o t h r i p s ramakrishnae, and S c h e d o t h r i p s s p . ( 2 1 ) . Vapors o f t h i s compound produced a dose-dependent r e p e l l e n c y i n workers o f two a n t s p e c i e s , Monomorium c a r b o n a r i u m and Iridomyrmex h u m i l i s , under l a b o r a t o r y c o n d i t i o n s . Thus, p e r i l l e n e f u n c t i o n s as a r e p e l l e n t and i t s p r e s e n c e i n t h e a n a l exudates o f d i v e r s e t h r i p s s p e c i e s c l e a r l y augments t h e d e t e r r e n t e f f i c a c i e s o f t h e s e d i s c h a r g e s . On t h e o t h e r hand, i t has been suggested t h a t h i g h dosages o f p e r i l l e n e (20-200 Mg) can f u n c t i o n as an a l a r m pheromone ( 1 7 ) . A t h i r d monoterpene, r o s e f u r a n , has been i d e n t i f i e d as t h e major c o n s t i t u e n t produced by t h e t h r i p s A r r h e n o t h r i p s r a m a k r i s h n a e (21^). Rose f u r a n i s accompanied by p e r i l l e n e and i n a d d i t i o n , hexadecyl acetate i s q u a n t i t a t i v e l y s i g n i f i c a n t . Two a r o m a t i c compounds, p h e n o l and p h e n y l a c e t a l d e h y d e , a r e minor c o n c o m i t a n t s i n t h e a n a l exudate.

CHO

Rose Furan

0-Acaridial

Perillene



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F a t t y acids are a l s o c h a r a c t e r i s t i c n a t u r a l products of s p e c i e s o f t h r i p s i n a d i v e r s i t y o f genera. A t o t a l e x t r a c t o f H o p l o t h r i p s j a p o n i c u s was dominated by ( E ) - 3 - d o d e c e n o i c a c i d w h i c h i s c o n s i d e r e d t o be an a l a r m - a g g r e g a t i o n pheromone; ( Z ) - 5 d o d e c e n o i c a c i d i s a minor c o n c o m i t a n t ( 2 2 ) . 2-Methylbutyric a c i d , a d e f e n s i v e allomone o f s w a l l o w t a i l l a r v a e ( 2 3 ) , i s the o n l y f r e e f a t t y a c i d d e t e c t e d i n the p r e v i o u s l y d e s c r i b e d a n a l exudate of Varshneyia p a s a n i i (20). I t i s b e l i e v e d t h a t the a n a l d i s c h a r g e o f t h i s s p e c i e s , t h o r o u g h l y dominated by a l k a n e s , a c e t a t e s , and oxygenated monoterpenes, e x h i b i t s an i n c r e a s e d r e p e l l e n t "punch" because o f t h e p r e s e n c e o f the C5 a c i d . The a n a l f l u i d o f a D i n o t h r i p s sp. c o n t a i n s o n l y i s o v a l e r i c and d e c a n o i c a c i d s i n e q u a l q u a n t i t i e s ( 2 4 ) . A c o m b i n a t i o n o f t h e a c i d s i s h i g h l y r e p e l l e n t t o workers of t h e f i r e ant S o l e n o p s i s i n v i c t a . Decanoic a c i d i s t h e major allomone p r e s e n t i n the a n a l f l u i d o f E u r y a p l o t h r i p s c r a s s u s and i s accompanied by dodecanoic a c i d as a q u a n t i t a t i v e l y i m p o r t a n t p r o d u c t ( 2 1 ) . The exudate o f E. c r a s s u s a l s o c o n t a i n s 2 - p h e n y l a c e t a l d e h y d e , p h e n o l , and 4o c t a d e c - 9 - e n o l i d e as minor c o n s t i t u e n t s . Dodecanoic a c i d has a l s o been i d e n t i f i e d as a major compound i n t h e a n a l exudate o f Elaphrοthrips t u b e r c u l a t u s , and i t i s accompanied by two o t h e r a c i d s , ( Z ) - 5 - t e t r a d e c e n o i c a c i d and 5,8t e t r a d e c a d i e n o i c a c i d ( 2 5 ) . On t h e o t h e r hand, a n o v e l a n i m a l n a t u r a l p r o d u c t , j u g l o n e , p r o v i d e s t h i s exudate w i t h a p a r t i c u l a r l y d i s t i n c t i v e exocrine chemistry. Juglone, which i s s y n t h e s i z e d de novo by E. t u b e r c u l a t u s , i s an o u t s t a n d i n g r e p e l l e n t f o r ant s p e c i e s i n s e v e r a l genera. The a l l e l o p a t h i c e f f e c t s of j u g l o n e , a product of black walnut (Juglans n i g r a ) , are w e l l e s t a b l i s h e d ( 2 6 ) , and i t i s r e a l l y not s u r p r i s i n g t h a t t h i s h i g h l y p h y t o t o x i c and r e a c t i v e quinone s h o u l d e x h i b i t c o n s i d e r a b l e r e p e l l e n t a c t i v i t y f o r a n t s as a consequence of a s s a u l t i n g t h e i r chemoreceptors.

ο

ο

HO

Juglone


2.

BLUM E T A L



Honey Bee Pheromones as R e p e l l e n t s Some pheromones o f s o c i a l i n s e c t s w h i c h f u n c t i o n as e x c i t a n t s and a t t r a c t a n t s a t low ( = p h y s i o l o g i c a l ) c o n c e n t r a t i o n s a r e p o w e r f u l r e p e l l e n t s when p r e s e n t a t super t h r e s h o l d c o n c e n t r a t i o n s ( 2 7 ) . The a b i l i t y o f t h e s e i n s e c t s t o be d e t e r r e d by h i g h l e v e l s o f t h e i r own pheromones can p r o v i d e a means o f d e t e c t i n g new r e p e l l e n t s f o r e u s o c i a l a r t h r o p o d s . Beyond t h i s c o n s i d e r a t i o n , i t i s p o s s i b l e t h a t t h e s e "pheromonal r e p e l l e n t s " might s e r v e as r e p e l l e n t s f o r a wide range o f i n s e c t s . Honey bee workers u t i l i z e a mandibular g l a n d pheromone, 2heptanone, as a low l e v e l a l a r m pheromone a t t h e h i v e e n t r a n c e ( 2 8 ) . T h i s compound, w h i c h i s a r e p e l l e n t f o r f o r a g i n g worker bees ( 2 9 ) , produces abnormal b e h a v i o r a l r e a c t i o n s when workers a r e exposed t o h i g h c o n c e n t r a t i o n s o f i t ( 3 0 ) , i n much t h e same way as i s observed w i t h 2-heptanone-producing a n t s ( 3 1 ) . S i g n i f i c a n t l y , when t h i s methyl ketone i s a p p l i e d t o t h e hands as a 0.5, 1.0, o r 2% a e r o s o l s o l u t i o n , i t i s p o s s i b l e t o m a n i p u l a t e t h e bees i n a h i v e w i t h o u t them r e a c t i n g a g g r e s s i v e l y . Workers a r e r e p e l l e d by t h e k e t o n i c super t h r e s h o l d c o n c e n t r a t i o n and r e t r e a t from i t s s o u r c e i n a n o n a g i t a t e d s t a t e . The h i g h c o n c e n t r a t i o n o f t h i s pheromone thus e f f e c t i v e l y disarms t h e workers and p r o v i d e s a r e p e l l e n t " s h i e l d " f o r t h e pheromone e m i s s i o n s o u r c e . S i n c e some cockroaches u t i l i z e 2-heptanone as a d e f e n s i v e allomone ( 3 2 ) , i t i s p o s s i b l e t h a t t h i s compound may be r e p e l l e n t t o a broad spectrum o f i n s e c t s p e c i e s . Young honey bee queens produce a r e p e l l e n t pheromone t h a t e f f e c t i v e l y t r a n q u i l i z e s workers t h a t may i n t e r a c t a n t a g o n i s t i c a l l y w i t h t h e s e v i r g i n females ( 1 6 ) . The a c t i v e compound, o-aminoacetophenone, i s a minor component i n t h e a n a l exudate t h a t i s d i s c h a r g e d by t h e molested queens ( 3 3 ) . T h i s compound i s a l s o a d e f e n s i v e allomone o f an a n t s p e c i e s ( 3 4 ) , r a i s i n g t h e p o s s i b i l i t y t h a t i t may possess g e n e r a l d e t e r r e n t a c t i v i t y f o r arthropods.

o-Aminoacetophenone


20



The R e p e l l e n c y of Venomous A l k a l o i d s o f A n t s A n t s i n t h e myrmicine genera S o l e n o p s i s and Monomorium a r e d i s t i n c t i v e i n p r o d u c i n g venoms t h a t a r e dominated by a l k a l o i d s r a t h e r than p r o t e i n s ( 3 5 ) . F i r e a n t s ( S o l e n o p s i s spp.) i n t h e subgenus S o l e n o p s i s c h a r a c t e r i s t i c a l l y s y n t h e s i z e p o i s o n g l a n d s e c r e t i o n s t h a t a r e dominated by t h e c i s - and t r a n s - i s o m e r s o f 6a l k y l - o r 6 - a l k y l i d e n e - 2 - m e t h y l p i p e r i d i n e s ( 3 6 ) . On t h e o t h e r hand, s p e c i e s i n t h e subgenus D i p l o r h o p t r u m f r e q u e n t l y produce 2 , 5 - d i a l k y l p y r r o l i d i n e s as venomous c o n s t i t u e n t s ( 3 7 ) , as w e l l as 3 , 5 - d i a l k y l p y r r o l i z i d i n e s ( 3 8 ) , and 3 , 5 - d i a l k y l i n d o l i z i d i n e s ( 3 9 ) . The venoms o f Monomorium s p e c i e s t y p i c a l l y c o n t a i n 2,5d i a l k y l p y r r o l i d i n e s t h a t a r e f r e q u e n t l y accompanied by 3,5d i a l k y l p y r r o l i z i d i n e s and 3 , 5 - d i a l k y l i n d o l i z i d i n e s (AO, 41, 4 2 ) . With the exception of the d i a l k y l p i p e r i d i n e s (reviewed i n 14), v i r t u a l l y n o t h i n g i s known about t h e b i o l o g i c a l a c t i v i t i e s o f t h e o t h e r c l a s s e s o f venomous n i t r o g e n h e t e r o c y c l e s . In view of the r e p o r t e d d e t e r r e n t a c t i v i t i e s of Solenopsis and Monomorium venoms under f i e l d c o n d i t i o n s (10, 11, 1 2 ) , i t seemed w o r t h w h i l e t o e v a l u a t e t h e comparative r e p e l l e n c i e s t o a n t s o f some o f t h e s e venom-derived a l k a l o i d s . I n t h i s i n v e s t i g a t i o n , t h e d e t e r r e n c y of t h e s e n i t r o g e n h e t e r o c y c l e s t o a v a r i e t y o f ant s p e c i e s was determined by u s i n g a f e e d i n g b i o a s s a y i n w h i c h t h e r e a c t i o n s o f hungry ant w o r k e r s t o a l k a l o i d - t r e a t e d f o o d were q u a n t i f i e d ( 4 3 ) . S e l e c t i o n o f a v a r i e t y o f a g g r e s s i v e ant s p e c i e s i n c o m b i n a t i o n w i t h a d i v e r s i t y of c a n d i d a t e compounds, b e l o n g i n g t o t h e main c l a s s e s o f venomous a l k a l o i d s , p r e s e n t e d an o p p o r t u n i t y t o examine t h e s e f o r m i c i d n a t u r a l p r o d u c t s i n terms o f t h e i r a c t i v i t i e s as r e p e l l e n t s . Queenright ( q u e e n - c o n t a i n i n g ) c o l o n i e s of 10 s p e c i e s of a n t s , b e l o n g i n g t o two major s u b f a m i l i e s , were u t i l i z e d f o r r e p e l l e n c y s t u d i e s . Members o f t h e s u b f a m i l y M y r m i c i n a e i n c l u d e d S o l e n o p s i s i n v i c t a , Crematogaster ashmeadi, P h e i d o l e d e n t a t a , Monomorium minimum, M. v i r i d u m and M^ p h a r a o n i s . The s u b f a m i l y D o l i c h o d e r i n a e was r e p r e s e n t e d by Iridomyrmex p r u i n o s u s , I . h u m i l i s , Tapinoma s e s s i l e , and T^ melanocephalum. Whereas S. i n v i c t a and t h e Monomorium s p e c i e s have been demonstrated t o s y n t h e s i z e a l k a l o i d - r i c h venoms (36, 40, 41_), t h e s e n i t r o g e n h e t e r o c y c l e s have n o t been d e t e c t e d as p o i s o n g l a n d p r o d u c t s o f any o f t h e o t h e r myrmicine genera ( 4 4 ) . S i n c e we have f r e q u e n t l y o b s e r v e d workers s e c r e t i n g venom d u r i n g c o m p e t i t i v e i n t e r a c t i o n s between M^ p h a r a o n i s , M. v i r i d u m , and T^_ melanocephalum i n s o u t h e r n F l o r i d a , and t h e o t h e r seven s p e c i e s i n n o r t h e r n G e o r g i a , t h e s e s p e c i e s seemed p a r t i c u l a r l y a p p r o p r i a t e f o r e v a l u a t i n g t h e p o t e n c i e s o f t h e s e a l k a l o i d s as ant r e p e l l e n t s . B o t h f o r a g i n g and f e e d i n g were s t i m u l a t e d by not p r o v i d i n g t h e ant c o l o n i e s w i t h f o o d f o r 48 hours. Food was then o f f e r e d t o t h e a n t s as d r o p l e t s o f honey t o w h i c h were added 1 o r 2 pg o f a l k a l o i d s i n 2 μΐ o f a b s o l u t e e t h a n o l . I n one s t u d y , b o t h t r e a t e d d r o p l e t s and c o l o n i e s were randomized f o r each r e p l i c a t e w h i c h compared t h e r e p e l l e n c i e s o f f o u r a l k a l o i d s t h a t i n c l u d e d a S o l e n o p s i s a l k a l o i d , t r a n s - 6 - u n d e c y l - 2 - m e t h y l p i p e r i d i n e ( 3 6 ) , two Monomorium d i a l k y l p y r r o l i d i n e s ( 4 1 ) , and a S o l e n o p s i s d i a l k y l p y r r o l i z i d i n e ( 3 8 ) . I n t h i s i n v e s t i g a t i o n , a l l s p e c i e s of



2.

BLUM ET A L


a n t s were u t i l i z e d except p h a r a o n i s , T. melanocephalum, and I» h u m i l i s . A second r e p l i c a t e o f t h e measurements was performed 24 hours l a t e r , w i t h t h e same c o l o n i e s and b a i t s randomized i n a different pattern. I n a second s t u d y , t h e comparative d e t e r r e n c i e s o f e i g h t S o l e n o p s i s d i a l k y l p i p e r i d i n e s (36) and two S o l e n o p s i s d i a l k y l i n d o l i z i d i n e s (39) were compared. T e s t s p e c i e s i n c l u d e d two a l k a l o i d p r o d u c e r s , p h a r a o n i s and S^ i n v i c t a , and two s p e c i e s t h a t do not s y n t h e s i z e a l k a l o i d a l p o i s o n g l a n d s e c r e t i o n s , I . h u m i l i s and T^ melanocephalum (45, 4 6 ) . T h i s s t u d y , w h i c h was implemented t h e same way as d e s c r i b e d f o r t h e p r e v i o u s t e s t , was a l s o d e s i g n e d t o compare t h e d e t e r r e n t a c t i v i t i e s o f t h e c i s - and t r a n s - 2 , 6 - d i a l k y l p i p e r i d i n e s ( r e l a t i o n o f s u b s t i t u e n t s a t C-2 and C-6). I n c l u d e d were compounds i n w h i c h t h e 6 - a l k y l group was normal Cg, C^3, and C ^ ; t h e 6 - a l k y l i d e n e group was e i t h e r Z-4t r i d e c e n y l o r Z-6-pentadecenyl. Compounds a r e r e f e r r e d t o as c i s o r t r a n s i n c o m b i n a t i o n w i t h an a b b r e v i a t i o n f o r t h e c h a i n l e n g t h ( p l u s u n s a t u r a t i o n ) o f t h e group a t t a c h e d t o C-6. Thus, c i s - 6 n o n y l - 2 - m e t h y l p i p e r i d i n e ( I ) i s d e s i g n a t e d as c i s - C g and 2 - t r a n s 6-(4-tridecenyl)-2-methylpiperidine ( I I ) i s designated trans-C-^.^ ( F i g u r e 1 ) . Two d i a l k y l i n d o l i z i d i n e s , ( 5 Z , 9 Z ) - 3 - h e x y l - 5 m e t h y l i n d o l i z i d i n e (Hex Ind) and ( 5 Z , 9 Z ) - 3 - e t h y l - 5 m e t h y l i n d o l i z i d i n e ( E t I n d ) , were i n c l u d e d f o r comparison. Three r e p l i c a t e s o f t h e measurements were performed i n t h e s t u d y , u s i n g d i f f e r e n t random c o m b i n a t i o n s o f c o l o n i e s and t r e a t m e n t s , a t 7-10 day i n t e r v a l s .

CH

3

ι

H

trans-C

1 3 ; 1

(I)

F i g u r e 1. F o r t h e most p a r t , each o f t h e seven ant s p e c i e s e x h i b i t e d c h a r a c t e r i s t i c responses t o t h e f o u r a l k a l o i d s e v a l u a t e d i n t h e f i r s t s t u d y . For a l l s p e c i e s , a 2 pg dosage o f an a l k a l o i d was s i g n i f i c a n t l y more r e p e l l e n t t h a n 1 pg. However, workers o f f o u r o f t h e s p e c i e s , C^ ashmeadi, I . p r u i n o s u s , M. minimum, and M. v i r i d u m , were r e p e l l e d by each o f t h e a l k a l o i d s o f b o t h c o n c e n t r a t i o n s . Two of t h e compounds, 2 - ( l - h e x - 5 - e n y l ) - 5 n o n y l p y r r o l i d i n e ( I I I ) and 2 - ( l - h e x - 5 - e n y l ) - 5 - ( l - n o n - 8 e n y l ) p y r r o l i d i n e ( I V ) , were s i g n i f i c a n t l y more r e p e l l e n t than


21

22



( 5 Z , 8 E ) - 3 - h e p t y l - 5 - m e t h y l p y r r o l i z i d i n e (V) f o r a l l s p e c i e s ( F i g u r e 2 ) . The trans-C-Q p i p e r i d i n e ( V I ) was i n t e r m e d i a t e i n r e p e l l e n c y between the p y r r o l i d i n e s I I I and IV, and the p y r r o l i z i d i n e ( V ) , but was not s i g n i f i c a n t l y d i f f e r e n t from e i t h e r c l a s s of a l k a l o i d s (43).

The s p e c i e s t h a t do not produce a l k a l o i d - r i c h venoms--C. ashmeadi, T, s e s s i l e , I . p r u i n o s u s , and dentata--were s i g n i f i c a n t l y more r e p e l l e d by t h e s e n i t r o g e n h e t e r o c y c l e s than t h e t h r e e a l k a l o i d - s y n t h e s i z i n g s p e c i e s ( T a b l e 1 ) . These r e s u l t s suggest t h a t s p e c i e s t h a t g e n e r a t e venoms dominated by a l k a l o i d s may have a c o m p e t i t i v e advantage a g a i n s t s p e c i e s t h a t do not produce p o i s o n g l a n d s e c r e t i o n s c o n t a i n i n g t h e s e v o l a t i l e - - a n d r e p e l l e n t - - n a t u r a l products. Recent f i e l d s t u d i e s (47) s u p p o r t t h i s conclusion. I n t h e second s t u d y , w h i c h u t i l i z e d two s p e c i e s not known t o produce a l k a l o i d a l venoms--I. h u m i l i s and Ί\_ melanocephalum--and two a l k a l o i d - p r o d u c i n g s p e c i e s , M. p h a r a o n i s and S^ i n v i c t a , dosedependent r e s p o n s e s were o n l y o b s e r v e d f o r two o f the s p e c i e s w i t h s e l e c t e d d i a l k y l p i p e r i d i n e s ( 4 3 ) . The responses o f workers o f M. p h a r a o n i s t o the c i s - C p p i p e r i d i n e and the c i s - C ^ p i p e r i d i n e were c l e a r l y dose dependent, as was the response of workers of T. melanocephalum t o the c i s - C - ^ p i p e r i d i n e .


In Naturally Occurring Pest Bioregulators; Hedin, P.; ACS Symposium Series; American Chemical Society: Washington, DC, 1991. 3

Pyrrolidine^ 46.1 ± 5.3 15.2 ± 3.3 27.6 ± 3.4

c

2-(1-hex-5-enyl)-5-nonylpyrrolidine. ^2-(l-hex-5-enyl)-5-(l-non-8-enyl)pyrrolidine. ( 5 Z , 8E ) - 3-hepty1-5-methylpyrrο1i ζ i d i n e . ^trans-6-undecy1-2-methylp i p e r i d i n e .

a

Pyrrolidine A l k a l o i d producers 46.8 ± 6.6 N o n a l k a l o i d p r o d u c e r s 15.5 ± 3.4 A l l species 28.0 ± 3.8

c

Pyrrolizidine Piperidine^ 60.5 ± 8.0 53.2 ± 8.0 36.4 ± 1.6 28.9 ± 5.3 46.0 ± 5.1 37.4 ± 4.7

Alkaloid

Table 1. Mean number of ant workers (as percent of controls) of alkaloid- and nonalkaloidproducing species feeding on baits treated with four ant-derived alkaloids.


24


Workers o f b o t h melanocephalum and 1^ h u m i l i s , s p e c i e s t h a t do n o t produce a l k a l o i d a l venoms, were e s p e c i a l l y s e n s i t i v e t o t h e d e t e r r e n t e f f e c t s o f d i f f e r e n t a l k a l o i d s ; S^ i n v i c t a w o r k e r s were n o t r e p e l l e d by any o f t h e a l k a l o i d s ( T a b l e 2 ) . Workers o f p h a r a o n i s were n o t r e p e l l e d as e f f e c t i v e l y as t h o s e o f t h e two n o n a l k a l o i d - p r o d u c i n g s p e c i e s ( 4 4 ) . The r e p e l l e n c i e s o f t h e a l k a l o i d s f o r t h e s e n s i t i v e s p e c i e s were: c i s - C | 3 ι > c i s - C | 3 > cis-Cp > trans-C^3 > c i s - C i 5 . ^ > t r a n s - C j ^ . ^ > Hex I n d > t r a n s - C j 5 > c i s - C > E t I n d > EtOH ( s i g n i f i c a n t a t 5% level). These r a n k i n g s were o b t a i n e d u s i n g Duncan's M u l t i p l e Range T e s t on t h e numbers o f a n t s f e e d i n g a t each b a i t , e x p r e s s e d as p e r c e n t a g e s o f t h e a v e r a g e number o f a n t s from t h e i r c o l o n y f e e d i n g a t c o n t r o l b a i t s (see Table 1 ) . P a i r w i s e comparison o f t h e r e p e l l e n c i e s o f t h e c i s and t r a n s - i s o m e r s o f t h e 0 ^ 3 , C^5 and C^.^ d i a l k y l p i p e r i d i n e s demonstrated t h a t t h e c i s i s o m e r s o f t h e C^3 and C^.^ a l k a l o i d s a r e more r e p e l l e n t t h a n t h e i r t r a n s c o u n t e r p a r t s . On t h e o t h e r hand, no s i g n i f i c a n t d i f f e r e n c e s i n t h e d e t e r r e n c i e s o f t h e c i s and t r a n s - C ^ 5 compounds were o b s e r v e d . ;


1 5

Table 2. Mean number of ant workers (as percent of controls [EtOH]) of alkaloidand nonalkaloid-producing species feeding on baits treated with 10 ant-derived alkaloids.

Alkaloid

3

A l k a l o i d Producer

cis-C^3 cis-Cp cis-Cj^.ι trans-C-^ 3 c_is-C].5 EtOH trans-C^5 2 trans-CjL5 EtOH Hex I n d CIS-C13.2 Et Ind :

a

61.1 69.9 68.8 73.1 86.7 99.5 92.0 86.0 100.5 84.3 57.2 86.7

+ 8.2 ± 12.3 ± 5.8 ± 10.4 ± 7.1 ± 7.1 ± 8.0 ± 9.0 ± 9.0 ± 6.8 ± 8.9 ± 5.8

N o n a l k a l o i d producer 7.5 3.8 25.1 14.8 49.9 103.8 30.4 41.1 96.2 40.8 0.5 94.4

± ± ± ± ± ± ± ± ± ± ± ±

2.1 2.2 3.8 3.6 6.0 6.0 5.2 5.0 7.7 6.3 0.2 7.6

S e e t e x t f o r f u l l names o f a l k a l o i d s . Conclusions R e p e l l e n t compounds appear t o commonly f o r t i f y t h e e x o c r i n e secretions of a d i v e r s i t y of arthropods. As i l l u s t r a t e d by t h e d e t e r r e n t s s y n t h e s i z e d by t h r i p s , bees, and a n t s , c o n s i d e r a b l e s t r u c t u r a l e c l e c t i c i s m c h a r a c t e r i z e s t h e s e n a t u r a l p r o d u c t s . The g r e a t v a r i e t y o f d e f e n s i v e a l l o m o n e s w h i c h has been e v o l v e d t o blunt the a s s a u l t s o f m u l t i f a r i o u s predators a t t e s t s t o both the b i o s y n t h e t i c v i r t u o s i t y o f i n s e c t s and t h e w e a l t h o f p o t e n t i a l candidate r e p e l l e n t s . I t would be no e x a g g e r a t i o n t o s t a t e t h a t t h e i n c r e d i b l e s u c c e s s o f i n s e c t s i s i n no s m a l l way due t o t h e i r a b i l i t y t o e f f e c t i v e l y counter, w i t h chemical a r s e n a l s , the predatory


2. BLUM ET AL.


e f f r o n t e r i e s o f t h e i r enemies. These a l l o m o n a l d e t e r r e n t s have been " t r i e d and t e s t e d " i n t h e f u l l n e s s o f e v o l u t i o n a r y t i m e , and o f f e r humankind a t r e a s u r e t r o v e o f proven r e p e l l e n t s w i t h w h i c h to challenge pest species. I t i s time t o g i v e these arthropods c r e d i t f o r h a v i n g p e r f e c t e d c h e m i c a l w a r f a r e , and t o e x p l o i t t h e defensive products o f t h e i r success f o r s o c i e t y ' s b e n e f i t . L i t e r a t u r e Cited 1.


2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.

16. 17. 18. 19. 20. 21. 22. 23. 24.

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Arthropod Natural Products as Insect Repellents - American Chemical

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