A Comparison of Yeast Communities Found in Necrotic Tissue of Cladodes and Fruits of Opuntia

8/18/2019 A Comparison of Yeast Communities Found in Necrotic Tissue of Cladodes and Fruits of Opuntia

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Microb Ecol (1987) 14:179-192

M I C R O B I L E C O L O G Y

9 Springer-VerlagNew York Inc. 1987

C o m p a r is o n o f Y e a s t C o m m u n i ti e s F o u n d i n N e c r o t i c T i s s u e o f

C l a d o d e s a n d F r u i t s o f pun t ia st r i c ta on I s lands in t he

C a r i b b e a n S e a a n d W h e r e I n tr o d u c e d i n to u s t r a l ia

William T. Starmer, ~ Marc-Andre Lachance, 2 and Her man J. Phaff 3

~Department of Biology, Syracuse University, Syracuse, NY 13210, USA; 2Departrnent of Plant

Sciences, University of Western Ontario, London, Ontario N6A 5B7, Canada; and ~Department

of Food Scienceand Technology,University of California-Davis, Davis, California 95616, USA

Abs t r a c t

Yeast communities growing in the decaying tissues (cladodes

and fruits) of

Opuntia stricta

(prickly pear cactus) and associated yeast

vectors

Drosophila

species) were co mpared in two geographic regions (Ca-

ribbean and eastern Australia). The Australian yeast com mun ity provides

an interesting comparison to the Caribbean community, because the host

plant O.

stricta

was introduced to Australia over 100 years ago. Many of

the yeasts found in the Australian system also were introduced during a

period o f biological control (1926-1935) when they a ccompanied rotting

prickly pear cladodes and insects shipped to Australia from the Americas.

The yeast commu ni ty co mposit ion (propor tion of each species) is compar ed

at several levels of organization: (1) within and between regions, (2) across

seasons and years, and (3) within and between tissue types. The yeast species

compos ition of the cladode c ommuni ties are similar from locality to lo-

cality, season to season, and year to year, with the region-to-region simi-

larity slightly less. The composition of the fruit-yeast communities are

distinct from region to region and only show some overlap with the cladodes

within regions when collected simultaneously in the same locality. It is

suggested that the

cladode-microorganism-Drosophila

system is relatively

closed (little extrinsic influence) whereas the

fruit-microorganism-Dro-

sophila

system is open (large extrinsic influence).

I n t r odu c t i on

The compo sitio n of communitie s, in terms o f species present and their pro-

portional representation, is interesting from two standpoints. One is an evo-

lutionary view of how and why a comm un ity arrives at a certain state (mem-

bership and relative numbers of species) over man y generations. Thus, stasis

and change are under the influences of evolutionary forces such as natural

selection and chance. Ano the r is an ecological view o f how and why a com-

muni ty is found at a certain state at a particu lar time (e.g., within a generation

where time is short o n the evolut ionary scale). Thus, env ironm ental constraints,

species-species interactions (e.g., compe tit ion or facilitation), predation, succes-


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180 W.T. Starmer et al.

sional factors, and chance may play a role in shaping the community. The

objective o f this study was to try to evaluate the role o f the extrinsic environ-

ment on the composition of yeast communities. We compared the yeast com-

munitie s found in the decaying tissues of O p u n t i a s tr ic t a prickly pear cactus)

in their endemic environment s Pan-Caribbean) to communi ties found in an

introduced envir onment Australia). Some o f the Australian localities are cli-

matically different from those of the endemic populations, being at higher

elevations and higher latitudes [12]. In addition, the indigenous yeast species

in the local envi ronmen t may influence the new communitie s in the introduced

habitat.

Decaying cladodes or pads of O. s t r i c ta are utilized for feeding and breeding

by a number of insects including drosophilids. In the Caribbean,

D r o s o p h i l a

m u l l e r i , D . m a y a g u a n a ,

undescribed species

S . D . s ta lker i ,

and

D . r i c h a r d s o n i

are all found to various degrees in decaying cladodes W. B. Heed, unpubli shed

data). In Australia, both

D . b u z z a t i i

and

D . a l d r i c h i

are known to use the

cladodes but

D . b u z z a t i i

is more c ommo n and widespread [ 1, 2]. In both regions

fresh, healthy

O p u n t i a s t r i c t a

cladode tissue is attacked by the phycitid moth

C a c t o b l a s t i s c a c t o r u m ,

and rot initiation is thought to be principally due to

this primary herbivore. The resulting damaged tissue is then utilized by a

community of bacteria, yeasts, and molds on which the drosophilids and some-

times other insects feed, breed, and subsequently vector the microorganisms

to new rots.

The fruits of O.

s t r i c ta

are seasonal, they mature in autumn or winter [6].

The fruits are deciduous, but rotting often begins on the plant after lesions are

made by birds foraging on the succulent tissue. The holes left by birds are then

occupied by insects, including ants, beetles, and dipterans, most notably dro-

sophilids. In the Caribbean, a number of D r o s o p h i l a species feed on the open

fruit and some breed there. However, some species that breed elsewhere will

also feed on this sugar-rich substrate and may be responsible for introducing

microorganisms from other sources. The situation in Australia is similar in

that birds may be primarily responsible for fruit damage, and several drosoph-

ilids endemic and introduced) , including the pad-breeding D . b u z z a t i i , will

feed on fruits.

The original introduct ion o f O.

s t r i c ta

into Australia is not certain, but it is

presumed to have come from the vicinity of trade ports in Texas, Florida and

Cuba [8]. The first record o f O p u n t i a s t r i c t a originally referred to as O. i n e r m i s ,

a synonym) appears to be that of a plant brought from Sydney to Scone, New

South Wales in 1839. However , this species is believed to have been growing

in cultivation at Parr amat ta near Sydney) prior to that date. Sydney was also

the source for introduction of the species to Queensland in 1843.

Introduction of various insects and the establishment of biological control

took place primarily in the years 1926 to 1930 when large shipments o f materia l,

including cut portions of prickly pear

O p u n t i a )

with accompanying insects

that feed on the cladodes eggs, larvae and adults), were sent from the Americas.

The last consignment arrived in December 1935. A total of 67 separate ship-

ments 59 from the United States and 8 from Argentina) included 1,230 cases

of material. The microbiota con tained in these shipments, along with the ac-

cidental D r o s o p h i l a , were probably the major source of the present day com-


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C o m p a r i s o n o f Y e a s t C o m m u n i t i e s i n N e c r o ti c T i s su e 1 81

m u n i t i e s o f y e a s t s . W e t h e r e f o r e p r e s u m e t h e y e a s t c o m m u n i t i e s o f O .

stricta

i n A u s t r a l i a t o b e a c o m p o s i t e o f s p e c i e s f r o m b o t h A m e r i c a n c o n t i n e n t s .

F u r t h e r m o r e , t h e c o m m u n i t i e s f o u n d i n t h e C a r i b b e a n a r e t e n t a t i v e l y c o n s i d -

e r e d t o b e e n d e m i c t o t h a t r e g i o n . I t i s o f i n t e r e s t t h a t

actoblastis cactorum

( i n d i g e n o u s t o S o u t h A m e r i c a ) f o u n d i n t h e C a r i b b e a n w a s s u b s e q u e n t l y i n -

t r o d u c e d t o t h a t r e g i o n f r o m A u s t r a l i a [ 9 , 1 1 - 1 3 ] a n d t h a t p o p u l a t i o n s o f O .

stricta i n t h e C a r i b b e a n a r e n o w u n d e r t h i s s i m i l a r s e l e c t i v e p r e s s u r e . I n t r o -

d u c t i o n o f

actoblastis cactorum

f r o m A u s t r a l i a t o t h e C a r i b b e a n i n 1 9 5 7 w a s

v i a e g g s t i c k s ( w h i c h m a y n o t c a r r y y e a s t s ) a n d n o t b y s h i p m e n t o f r o t t i n g

m a t e r i a l s [ 9 ] .

a t e r i a ls a n d e t h o d s

S a m p l e s o f n e c r o ti c O .

stricta

t i s s u e ( c l a d o d e s a n d f r u i t s ) w e r e c o l l ec t e d f r o m 2 0 d i s t i n c t l o c a li t ie s

( 1 4 f r o m v a r i o u s C a r i b b e a n i s l a n d s , 6 f r o m e a s t e r n A u s t r a l i a ) . T h e s e c o l l e c t i o n lo c a l i ti e s a r e l is t e d

i n T a b l e i a l o n g w i t h t h e d a t e a n d n u m b e r o f s a m p l e s . T h e c o l l ec t io n l o ca l it ie s i n t h e C a r i b b e a n

r e g i o n w e r e p o o l e d a c c o r d i n g to p r o x i m i t y (e .g ., s a m e i s l a n d ) t o f o r m 8 C a r i b b e a n l o c a li t ie s . T h e

C a r i b b e a n c o l le c ti o n s w e r e m a d e i n M a y 1 9 82 d u r i n g cr u is e C F - 8 2 0 5 a n d i n N o v e m b e r 1 9 83

d u r i n g c r u i s e C F - 8 3 1 4 o f t h e r e s e a r c h v e s se l C a p e F l o r i d a i n t h a t r e g io n .

S a m p l e s w e r e t a k e n b y r e m o v i n g s e v e r a l g r a m s o f d e c a y in g t i ss u e f r o m t h e i n f e c te d c la d o d e s o r

f r u i ts o f i n d i v i d u a l p la n t s . N o m o r e t h a n o n e s a m p l e p e r p l a n t w a s t a k e n . E a c h t is s u e s a m p l e w a s

p l a c e d i n a s t er il e W h i r l - p a k b a g a n d s t o r e d i n a c o o l b o x ( 4 - 1 0 ~ u n t i l r e t u r n to t h e l a b o r a t o r y

f o r p la t in g . P l a t in g t o o k p l ac e f r o m 2 - 8 h o u r s a f t e r c o l le c ti o n . H o m o g e n a t e s w e r e p r e p a r e d b y

p l a c in g 1 g o f th e d e c a y i n g t is s u e i n t o 9 m l o f s t er il e w a t e r a n d v o r t e x i n g f o r 1 m i n . D i l u t i o n s o f

e a c h h o m o g e n a t e w e r e m a d e i n s te p s o f 1 / 1 0 in s t e ri le w a t e r fo l lo w e d b y p l a ti n g 0,1 m l o f v a r i o u s

d i l u t i o n s a s p r e v i o u s l y d e s c r i b e d [ 1 5 ] . I n s o m e c a s e s o n e l o o p f u l ( 0 .0 1 - - 0. 0 2 m l ) o f th e o r i g i n a l

h o m o g e n a t e w a s d i r e ct ly s t r e a k e d o n t h e i s o la t io n p l a t e . P l a t in g w a s c o n d u c t e d o n a c id i f ie d ( to

p H 3 . 8 w i t h 1 N H C 1) y e a s t e x t r a c t - m a l t e x t ra c t a g a r ( Y M , D i fc o ) , a n d i n c u b a t i o n w a s a t r o o m

t e m p e r a t u r e (2 5 ~ A r e p r e s e n t a t iv e o f e a c h c o l o n y ty p e f r o m e a c h s a m p l e w a s r e s t re a k e d o n c e

o r t w i c e a n d t h e r e s u l ti n g c u l t u r e w a s i d e n ti f ie d b y s t a n d a r d r e c o m m e n d e d p r o c e d u r e s [ 16 ]. F r e -

q u e n c y o f is o l a ti o n w a s d e t e r m i n e d o n a p e r p l a n t b a s is b y d i v i d i n g t h e n u m b e r o f p la n t s co n t a i n in g

a p a r t i c u l a r y e a s t b y t h e n u m b e r o f p l a n t s s a m p l e d . S o m e i n f o r m a t i o n i s l o s t b y t h i s p r o c e d u r e

b u t w e h a v e e m p l o y e d i t s o t h a t e a r li e r w o r k o n t h e A u s t r a l i a n m i c r o b i o t a [ 3, 4] c o u l d b e u s e d i n

d i r e c t c o m p a r i s o n . I n a d d i t io n , s e v e r a l c o m p l i c a t in g f a c to r s s u c h a s d i f fe r e n ce s in r o t m o i s t u r e ,

v a r i a b l e a d h e r e n c e o f y e a s t c e ll s, a n d i n a b i l it y to e q u a l l y h o m o g e n i z e a ll r o t s a m p l e s m a d e w i t h i n -

s a m p l e e s t i m a t e s o f y e a st n u m b e r s l es s r e li a b le . W e h a v e t h e r e f o r e fo c u s e d o u r a t t e n t i o n o n

s a m p l i n g y e a s t c o m m u n i t i e s w i t h i n a l o c a li ty . S i m i l a r it y o f tw o y e a s t c o m m u n i t i e s w a s c a l c u la t e d

a s P e a r s o n s p r o d u c t m o m e n t c o r r e l a t i o n c o e f fi c ie n t ( r) . T h o s e l o c a l it i e s t h a t y ie l d e d l e ss t h a n 1 5

y e a s t i s o l a t e s f r o m a p a r t i c u l a r s u b s t r a t e w e r e n o t i n c l u d e d i n t h e s i m i l a r i t y a n a l y s i s ( i . e . , p a d

l o c a l it i e s 3, 1 1; f ru i t l o c a li t ie s 4 , 6 , 7 ). T h e p h y s i o l o g i c a l s tr u c t u r e o f y e a s t c o m m u n i t i e s w a s a n a l y z e d

b y t h e m e t h o d o f L a c h a n c e a n d S t a r m e r [ 10 ], s u m m a r i z e d a s f o ll o w s. T h e s p e c i es f re q u e n c y m a t r i x

i s m u l t i p l ie d b y a m a t r i x o f p h y si o lo g i c al r e s p o n s e s o f t h e c o m p o n e n t y e a s t s pe c ie s , a n d e a c h

c o m m u n i t y i s t h e n d e s c r i b e d a s a v e c t o r o f m e a n p h y s i o l o g ic a l r e s p o n s e s. T h e r e s p o n s e s ar e

c o m p a r e d w i t h t h e e x p e c t e d m e a n r e s p o n s e s o f al l y e a s t sp e c ie s k n o w n ( d a t a f r o m B a r n e t t et al .

[ 5] ) a n d e x p r e s s e d as s t a n d a r d n o r m a l d e v i a t e s o f t h e i r e x p e c te d m e a n u s i n g a b i n o m i a l m o d e l f o r

s m a l l e r c o m m u n i t i e s a n d a n o r m a l a p p r o x i m a t i o n f o r la r g e r o n e s . A m e a n p h y s i o lo g i c a l r e s p o n s e

m a y t h e n b e v i e w e d a s n o t s i g n i f i ca n t , o r a s s i g n i f ic a n t l y l a r g e r o r s m a l l e r t h a n e x p e c t a t i o n f o r a

p a r t i c u l a r cr i ti c a l p r o b a b i l i t y (e .g ., 0 .0 5 ) . T h e p r o p o r t i o n o f c o m m u n i t y r e s p o n s e s t h a t a p p e a r

s i g n i f i ca n t b y t h i s a n a l y s i s i s g i v e n a s S . I n t h e p r e s e n t c a s e ,

Prototheca

e n t r i e s w e re d e l e te d f r o m

t h e d a t a b e c a u s e i t s c h a r a c t e ri s t ic s w e r e n o t i n c l u d e d i n t h e p h y s i o lo g i c a l d a t a b y B a r n e t t e t a l.

[ 5 ] . T h e e n t r y f o r f r u i t f r o m N a v a s s a I s l a n d i s d e l e t e d a l s o b e c a u s e i t i n c l u d e d o n l y o n e y e a s t

spec i e s .


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182

Table 1. Collection localities, dates, substrates, and numbers for

puntia stricta cladodes and fruits from two regions

No. of

samples

Clad-

Locality Date odes Fruits

(Caribbean Islands)

Haiti

Fond Parisi enne 5/6/82 13 0

Jacmel 5/7/82 5 0

Tota l 18 0

Spanish Pt., Monts erra t 5/15/82 17 0

British Virgin Islands

Beef Island 5/17/82 1 0

Virgin Gorda 5/18/82 3 0

Total 4 0

Little Conception Island, Bahamas l 1/18/83 16 3

Great Inagua, Bahamas 11/19/83 28 27

Navass a Island, U.S.A. 11/21/83 30 3

Jamaica

Discovery Bay I 1/23/83 15 l0

Sandy Bay 11/23/83 11 0

Palisadoes, Kingston 11/23/83 2 0

Total 28 10

Cayman Islands

Cayman Brac 11/25/83 16 15

Little Cayman Island 11/26/83 5 1

Grand Cayman Island 11/27/83 12 0

Total 33 16

(Australia)

O Har a (Denman) , N.S.W. 7/27/84 18 9

Breeza, N.S.W. 8/5/84 19 0

Metz Gorge, N.S.W. 8/9/84 8 12

Trinkey, N.S.W. 8/13/84 5 7

Hemm ant , Queensland 8/19/84 18 0

Lightning Ridge, N.S.W. 10/8/84 13 0

W. T. Starmer et al.

To produce a structured table of significantly deviating responses, the deviates were subjected

to bidimensio nal clustering by equally weighted pair agglomeration of a cosine matrix. A d endro -

gram shows the cluster structure (Fig. 1), and partit ions show groups of physiological responses

differing from one a nothe r by cosine values o f 0.8 or less.


5/14

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6/14

184 W .T . Starm er et al .

e s u l t s

T a b l e s 2 a n d 3 li st t h e p r o p o r t i o n s o f t h e y e a s t sp e c i e s f o u n d i n d e c a y i n g

c l a d o d e s a n d f ru i ts , r e s p e c t i v e l y . I t i s a p p a r e n t f r o m T a b l e 2 t h a t c e r ta i n c o m -

m o n y e a s t s in t h e C a r i b b e a n r e g i o n a r e r e s t r i c t e d t o t h a t a r e a ( i.e ., P i c h i a

n o r v e g e n s i s , P . a m e t h i o n i n a v a r . f , a n d th e l e ss c o m m o n P . m e x i c a n a ) a s

c o m p a r e d t o t h e A u s t r a l i a n c o l le c t i o n . I t s h o u l d b e n o t e d t h a t P . s p. B ' a n d

s t r a i n s b e l o n g i n g t o t h e C r y p t o c o c c u s c e r e a n u s c o m p l e x h a v e b e e n f o u n d i n

A u s t r a l i a i n p r e v i o u s s t u d ie s o f O . s t r i c ta y e a s t s [ 3 , 4 ]. T h e r e a s o n f o r r e f e r r i n g

i n T a b l e 2 t o t h e Cr . cereanus c o m p l e x r a t h e r th a n t o C r . c e r e a n u s ( o r i t s

t e l e o m o r p h S p o r o p a c h y d e r r n i a c e r e a n a ) i s t h a t th e G + C c o n t e n t s o f m a n y

i so l a t es w e r e f o u n d t o b e m u c h l o w e r th a n t h a t o f Cr . cereanus , s u g g e s t i n g t h a t

w e a r e d e a l i n g w i t h r e l a t e d b u t d i f f e r e n t s p e c i e s . S t r a i n s o f C l a v i s p o r a s p .

r e p o r t e d i n T a b l e 2 w e r e m a i n l y

C l a v i s p o r a o p u n t i a e

a n d a m i n o r n u m b e r o f

t h e r e l a t e d s p e c i e s

C l a v i s p o r a l u s i ta n i a e .

T h o s e c o m m o n y e a s t s f o u n d o n l y i n t h e A u s t r a l i a n s u r v e y b u t n o t in th e

C a r i b b e a n a re

P i c h i a o p u n t i a e ,

a n d t o s o m e e x t en t

H a n s e n u l a c a l i f o r n i c a , C a n -

d i d a b o i d i n i i , a n d K l o e c k e r a a p i c u l a t a . T h e l a s t sp e c ie s w a s f o u n d p r i m a r i l y i n

f r u it s a n d a p p e a r e d i n t h e c la d o d e s , i n l o w n u m b e r s , w h e n f r u it s w e r e p r e s e n t

( c o m p a r e T a b l e s 2 a n d 3 ). L o c a l i t y # 1 4 a l so h a d f r u it s p r e s e n t b u t t h e y w e r e

n o t s a m p l e d . B o t h H . c a l i f o r n i c a (a c o m m o n s o i l y e a st ) a n d C. bo id in i i ( o c -

c a s io n a l ly f o u n d i n c ac t u s r o ts ) w e r e r e c o v e r e d f r o m r o t t i n g c l a d o d e s i n M e t z

G o r g e , N . S . W . ( lo c a l it y # 1 1). T h i s l o c a l i ty d i d n o t h a v e

D r o s o p h i la b u z z a t i i

n o r C a c t o b l a s t i s c a c t o r u m p r e s e n t a n d s h o u l d b e c o n s i d e r e d a n e x c e p t i o n s in c e

i n a ll o t h e r A u s t r a l i a n l o c a l i t i e s D . b u z z a t i i a n d C . c a c t o r u m w e r e a c t i v e l y

f e e d i n g o n a n d v e c t o r i n g y e a s t s f r o m r o t t o r o t . W i t h t h i s i n m i n d , P . o p u n t i a e

a p p e a r s t o b e th e o n l y c o m m o n c l a d o d e y e a s t n o t f o u n d i n t h e C a r i b b e a n

c o m m u n i t i e s . T h e o r i g in o f P . o p u n t i a e i s u n c e r t a i n a s i t h a s n o t b e e n r e c o v e r e d

f r o m s o u r c e s i n t h e C a r i b b e a n , M e x i c o , o r t h e U n i t e d S t a te s . I t p o s s i b l y o r ig -

i n a t e d i n A r g e n t i n a w h e r e D . b u z z a t i i w a s p r e s u m e d t o o r i g i n a t e w h e n b i o l o g -

i ca l c o n t r o l w a s i n s t i t u t ed i n A u s t r a l ia . Y e a s t s th a t w e r e c o m m o n t o b o t h t h e

C a r i b b e a n i s l an d s a n d A u s t r a l i a i n c lu d e P i c h i a c a c t o p h i l a , C a n d i d a s o n o r e n s i s ,

a n d

C l a v i s p o r a

s p ., a n d t o a l e s s e r e x t e n t P . s p . B a n d

C r . c e r e a n u s

c o m p l e x

r e p o r t e d b y B a r k e r e t a l . [ 3 ] i n t h e i r e a r l i e r s u r v e y .

T h e y e a s t s p e c ie s f o u n d i n f ru i t o v e r l a p t o a l im i t e d d e g r e e w i t h t h e y e a s t s

o f c l a d o d e c o m m u n i t i e s . I n A u s tr a li a , P. opun t iae , w h i c h i s c o m m o n in c la d o d es ,

w a s a b s e n t f r o m f r u i t , w h e r e a s P . m e m b r a n a e f a c i e n s a n d P . n a k a s e i w e r e

r e c o v e r e d f r o m f r u it b u t n o t f r o m e l a d o d e r o t s . F u r t h e r m o r e , K l o e c k e r a a p i -

cu la ta , a v e r y c o m m o n f r u i t y e a s t , a p p e a r e d i n f r e q u e n t ly i n c la d o d e s a n d o c -

c u r r e d o n l y w h e n f r u it w a s p r e s e n t ( f ru i ts w e r e p r e s e n t a t l o c a l i ty # 1 4 b u t w e r e

n o t s a m p l e d ) . T h e C a r i b b e a n r e s u lt s f o r f r u i t a r e le ss c l e a r f o r t w o r e a s o n s : ( 1)

s o m e l o c a l i t i e s (# 4 , 6 , 7 ) w e r e n o t a d e q u a t e l y s a m p l e d , a n d ( 2) f r u i t f r o m l o c a l it y

# 8 w e r e g r e e n ( u n r i p e ) f ru i ts . T h i s l e a v e s o n e c o l l e c t io n ( # 5 ) f o r c o m p a r i s o n .

E x c l u d i n g t h o s e s p ec ie s w h i c h w e r e le ss t h a n 5 % o f t h e c o m m u n i t y , P. nor -

vegens i s i s c o m m o n i n b o t h s u b s t r a t e s . F o u r s p e c ie s a r e e i t h e r e x c l u s i v e to

c l a d o d e s C r . c e r e a n u s c o m p l e x ) , o r m o r e c o m m o n i n c l a d o d e s P. cac toph i la ,

C . sonorens i s ,

a n d

P r o t o t h e c a ) .

T h r e e s p e c ie s a re e i t h e r e x c l u s iv e to o r a r e m o r e

f r e q u e n t i n f r u i t s P i c h i a s p . B , C a n d i d a k r u s e i , a n d K l o e c k e r a a p i s ) . T w o


7/14

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8/14

186 W. T. Starmer et al.

Table 3. Relative frequency of yeast species isolated from fruits of Opuntia stricta collected at

localities (see Table 1) in the Caribbean and Australia

Caribbean Islands Australia

Yeast species Locality # 4 5 6 7 8 9 11 12

Pichia cactophila .2 .018 0 .167 .438 .045 0 0

P. norvegensis 0 .200 0 0 0 0 0 0

P. sp. B .2 .109 0 .167 0 0 0 0

P. kluyveri 0 0 0 0 0 .182 0 0

P. nakasei 0 0 0 0 0 .045 0 .333

P. membranaefaciens 0 .055 0 .167 0 .182 0 0

P. amethionina var. ameth. 0 0 0 0 0 .045 0 0

P. amethionina var. f ' .2 .036 0 .167 .063 0 0 0

Issatchenkia terricola 0 .036 0 0 0 0 0 0

Candida sonorensis 0 .036 0 0 .063 .045 0 .200

C. guilliermondii 0 .073 0 0 .188 0 0 0

C. parapsilosis 0 .018 0 0 0 0 0 0

C. stellata 0 .018 0 0 0 0 0 0

C. krusei 0 .127 0 0 0 0 0 .067

Clavispora sp. .2 .055 1 0 .25 .091 0 0

Torulaspora delbrueckii 0 .018 0 0 0 0 0 0

Saccharomyces cerevisiae 0 .018 0 0 0 0 0 0

Kloeckera apiculata 0 0 0 0 0 .273 .688 .400

K. apis 0 .145 0 .167 0 0 0 0

Hanseniaspora sp. 0 0 0 .167 0 0 0 0

Candida curvata .2 0 0 0 0 0 0 0

Cr. macerans 0 0 0 0 0 .045 0 0

Cr. hungaricus 0 0 0 0 0 .045 0 0

Cr. infirmo-miniatus 0 0 0 0 0 0 .313 0

Rhodotorula graminis 0 .018 0 0 0 0 0 0

Prototheca zopfii 0 .018 0 0 0 0 0 0

Total no. of isolates 5 55 2 6 16 22 16 15

less f requen t spec ies were found on ly o r more o f ten in f ru i t s P . me mb ra n a e -

fa c i e n s a n d C. gui l l iermondii) , wh i l e Clavispora sp . was in f requen t in bo th

c ladodes and f ru i t s in the Car ibbean . In Aus t ra l ia , Clavispora sp . was common

in c l a d o d e rot s , so m e t im e s r e p re se n t in g 5 0 % o r mo re o f t h e t o t a l y e as t p r e se n t

in an in d i v id u a l rot . I n su mm a ry , T a b le 4 li st s a q u a l i t a t i v e c o mp a r i s o n o f t h e

o v e r l a p b e twe e n the c o mm o n y e as t s (> 5 %) in t h e two c o mmu n i t i e s a n d two

reg ions . Th is tab le was cons t r uc te d by summ ing a ll i so la tes f ro m each loca l i ty

wi t h in a reg ion by subs t ra te , t hen no rma l iz ing by the to ta l num ber o f i so la tes .

The da ta o f Barker e t al . [3, 4] were inc luded . I t shou ld be no te d tha t bo t h P .

sp . 'B and Cr. cereanus c o mp le x h a v e b e e n i so l a t e d f ro m O. stricta c l a d o d e s

by Barke r e t a l. [3, 4] in Aus t ra l ia . Each o f these spec ies accou nte d fo r 4% o f

the i so la tes f rom O. stricta c ladodes in the i r l a rge su rvey .

S ta t i s t i c a l C o mp a r i so n s

T a b le 5 c o n ta in s s e v e ra l l e v e ls o f c o mp a ra t i v e in fo rm a t io n : (1) w i th in a n d

be tween subs t ra tes (c ladodes and f ru i t s ) , (2 ) wi th in and be tween reg ions (Ca-


9/14

C o m p a r i s o n o f Y e a s t C o m m u n i t i e s i n N e c r o t ic T i s su e 1 8 7

T a b l e 4 . Q u a l i t a ti v e c o m p a r i s o n o f th e o v e r la p b e t w e e n th e c o m m o n y e as ts (7 5 % o f t h e c o m -

m u n i t y ) o f t h e c l a d o d e a n d f ru i t c o m m u n i t i e s

O n l y i n M a i n l y i n

c l a d o d e s e l a d o d e s B o t h M a i n l y i n f r u it O n l y i n f r u it

C a r i b b e a n Cr. cereanus P. cactophila 1 . amethionina P. norvegensis

c o m p l e x ( v a t . f )

C. sonorensis Clavispora P.

s p . B

Prototheca P. membranae-

f ciens

C. guillier-

mondii

C. krusei

K. apis

A u s t r a l i a P. opuntiae P. cactophila P. kluyveri a K. apiculata ~ P. nakasei

C. sonorensis P. amethio- Cr. infirmo-

nina v a r . a . miniatus

Clavispora

sp .

P. membranae-

faciens

K i l l e r y e a s t s

r i b b e a n a n d A u s tr a li a ) , a n d 3 ) s e a s o n a l a n d b e t w e e n y e a r s . O u r p u r p o s e h e r e

w a s t o e s t a b l is h t h e e x t e n t o f s i m i l a r i t y b e t w e e n r e g i o n s a n d a s c e r t a i n w h a t

f a c t o r s m a y b e r e s p o n s i b l e f o r s i m i l a r i t i e s a n d d i f fe r e n c e s i n t h e s t r u c t u r e o f

t h e y e a s t c o m m u n i t i e s .

Y e a s t C o m m u n i t i e s o f C a c t u s C l a d o d es w i th i n R e gi o n s. P r e v i o u s w o r k [ 15 ] o n

O p un t i a phaeaca n t ha O . f icus - ind i ca

a n d O .

l i ndhe i m er i

s h o w e d t h a t y e a s t

c o m m u n i t i e s c o l le c te d f r o m t h e s a m e c a c t u s sp e c ie s a t t h e s a m e t i m e o f t h e

y e a r b u t f r o m s e p a r a t e l o c a l i t ie s h a v e s i m i l a r i t y c o e ff ic i en t s r a n g i n g f r o m a b o u t

r = 0 . 6 5 - 0 . 9 5 . S i m i l a r i t i e s b e t w e e n y e a s t c o m m u n i t i e s f r o m d i ff e re n t

O p u n t i a

s p e ci es w e r e s o m e w h a t l o w e r a p p r o x i m a t e l y 0 .6 0 ). T h e d a t a o f B a r k e r e t a l.

[3 ] w e r e a n a l y z e d i n a s i m i l a r m a n n e r a n d t h e a v e r a g e s i m i l a r i t y ac r o s s s e a s o n s

w i t h i n o n e l o c a l i t y 0 . 7 8 + 0 . 0 4 ; f r o m a l l s ix s e a s o n b y s e a s o n s i m i l a r i t i e s i n

T a b l e 5 ) w a s e s s e n t i a l l y t h e s a m e a s s i m i l a r i t i e s m e a s u r e d a c r o s s l o c a l i t i e s i n

o n e s e a s o n A u s t r a l ia , 1 9 8 4 ; r = 0 . 7 4 + 0 . 0 6 ; T a b l e 5 ). T h i s i n d i c a t e s t h a t

s p a t i a l a n d t e m p o r a l d i f f e re n c e s i n c o m m u n i t y c o m p o s i t i o n a r e o f s i m i l a r

m a g n i t u d e s f o r t h e i n t r o d u c e d y e a s t c o m m u n i t i e s f o u n d i n A u s t ra l ia . Y e a r - t o -

y e a r s i m i l a r i ty f o r t h e C a r i b b e a n c o m m u n i t i e s w a s e s t i m a t e d a t 0 .7 1 + 0 .0 5

T a b l e 5 ) w h i c h i s s i m i l a r t o w i t h i n - y e a r s i m i l a r i t y o f 0 . 7 9 a n d 0 . 7 3 + 0 . 0 7

T a b l e 5 ) f o r t h e s a m e r eg i on . T h e A u s t r a l ia n d a t a w e r e a l s o c o m p a r e d a c r o s s

y e a rs . T h i s c o m p a r i s o n s h o w e d a n a v e r a g e s i m i l a r i t y o f 0 .6 5 + 0 . 0 6 T a b l e 5)

f o r t h e y e a r s 1 9 77 a n d 1 9 8 4 . I t i s w o r t h n o t i n g t h a t t h e 1 9 8 4 d a t a w e r e c o l le c t e d

i n th e w i n t e r a n d s p r i n g a n d s h o w e d a n a v e r a g e s i m i l a r i t y o f 0 . 8 3 ___ 0 . 0 6 T a b l e

5 ) w i t h t h e 1 9 77 s p r i n g d a ta . I n b o t h r e g i o n s w e t h e r e f o r e s ee a b o u t t h e s a m e

a m o u n t o f y e a s t c o m m u n i t y s i m i l a r i t y f r o m l o ca l i t y to l o ca l i ty , s e a so n t o s ea -

s o n , a n d y e a r t o y e a r .


10/14

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11/14

Comparison of Yeast Communities n Necrotic Tissue 189

Yeast Communities of Cactus Cladodes between Regions.

The similarity be-

tween yeast communi ties f rom the Caribbean region and Australia is signifi-

cantly lower for each Caribbean collection of 1982 and 1983 compared to the

1984 Australian collection (0.50 _+ 0.06 and 0.49 _ 0.03, respectively; Table

5) but relatively higher compared to the 1977 Australian collection (0.62 +

0.18 a nd 0.77 ___0.06, respectively; Table 5). The decline for the 1984 Australian

collection mentioned above is primarily due to the low frequency of

P. cac-

tophila

and

Cr. cereanus

complex coupled with an increase in the frequency of

Clavispora sp. in that collection.

Yeast Communities of Cactus Fruit within and between Regions. The data for

fruit were not ob tained over seasons or years. To a large extent fruit are seasonal

and thi s precluded collection during certain t imes o f the year (i.e., May 1982;

Caribbean region). The Caribbean data are limited to two localities with ad-

equate sample size, one of which (Cayman Brac) was characterized by rotting

young green fruit still on the plant. These rots were dark yellow to brown, mos t

of which had not been opened by birds as is typical of ripe rotting fruit. Both

Caribbean yeast communities from fruit showed little similarity with those

observed in Australia (r = 0.004 +_ 0.04; Table 5). Within Australia the sim-

ilarity among communiti es in fruit (0.59 _+ 0.02; Table 5) was comparable,

although lower, to within-region (1984) similarities among yeast communiti es

in cladodes (0.74 _+ 0.06; Table 5). It therefore appears that the yeast com-

munities of fruits in the two regions are distinct and share little similarity.

Yeast Communities o f Cactus Cladodes and Cactus Fruits.

In bo th regions two

localities yielded data for which yeast communiti es o f fruits and cladodes could

be compared within the same locality. This within locality across substrate

comparison showed similarities (not shown in Table 5) of 0.33 (Great Inagua),

0.57 (Cayman Brac), 0.33 (O Hara), and 0.24 (Trinkey). This illustrates the

overlap between the substrates within a locality and in the case of the Cayman

Brac collection, shows the effect of green fruit on the overlap.

Compar isons a mong localities within regions show that the Caribbean yeast

communit ies o f fruits and cladodes do have significant similarities (0.37 _+

0.20 and 0.37 _+ 0.08; Table 5). By contrast, the Australian yeast communi tie s

show little across substrate similarities for any level of comparison (seasonal

data, r = 0.05-0.08; two years, r = 0.07-0.12; Table 5). The Australian yeast

communities of cactus fruit thus appear to be less linked to the yeast com-

munities of cactus cladodes, as compared to those in the Caribbean.

Yeast Community Physiology.

On the basis of physiology (Fig. 1), the yeast

communities associated with cladodes in the Caribbean appeared very ho-

mogeneous, and showed much resemblance with the Australian community

sampled at Breeza. The position ofcl adode s samples in Haiti in the dendrogram

is attributed to their lower proportion of

Candida sonorensis

their higher

proportion of P. mexicana and to the isolation from these samples of three

representatives of

Cryptococcus.

The yeasts isolated from cladodes at the other

five Austra lian sites (other than Breeza) fo rmed a separate cluster, characterized

by a higher-than-expected utilization ofxylose, xylitol, and ribitol, and to some


12/14

190 w .T . Starmer e t a l.

d e g re e , sa li ci n. I n m o s t o f t h e r e m a i n i n g c o m m u n i t i e s s t u d ie d , t h e s e c o m -

p o u n d s w e r e p o o r l y u t i l iz e d , o r t h e i r u t i l i z a t i o n w a s n o t u n u s u a l . T h i s is o b -

v i o u s l y li n k e d w i t h t h e f r e q u e n t is o l a t io n , i n A u s t r a l i a n c l a d o d e s , o f P . opun t i ae

( o n l y s a l i c i n ) , C. boidiniL o r C. muci lag ina . I t is d o u b t f u l t h a t t h i s t r e n d c o u l d

r e p r e s e n t a d if f e re n c e i n c a c tu s c h e m i s t r y . I n m a y , h o w e v e r , b e l i n k e d t o d i f -

f e r e n c e s i n n e i g h b o r i n g p l a n t s w h i c h c o u l d s e r v e a s i n o c u l a t i o n s o u r c e s.

T h e f r u i t y e a s t c o m m u n i t i e s a p p e a r e d l es s s t r u c t u r e d p h y s i o l o g ic a l ly , a s i n -

d i c a t e d b y t h e i r s p o r a d i c a p p e a r a n c e i n s e v e r a l c l u s t e r s ( F i g . 1 ) . I n g e n e r a l ,

t h e y d i f f er e d f r o m t y p i c a l c l a d o d e y e a s t s i n t h e i r d e c r e a s e d u s e o f l a c ti c a c id ,

e t h a n o l , a n d m e t h a n o l , a n d t o a c e r ta i n e x t en t , i n t h e m a x i m u m g r o w t h t e m -

p e r a tu r e s . T h e y e a s ts f o u n d i n c l a d o d e s t e n d e d t o e x h i b i t m o r e p o s i t iv e r e -

s p o n s e s t h a n e x p e c t e d f o r t h e s e f i v e c h a r a c te r i s t i c s . S u c h p a t t e r n s w e r e m u c h

l es s p r o n o u n c e d a m o n g f r u i t y e as ts . T h e o u t ly i n g p o s i t i o n o f t h e f r u it c o m -

m u n i t y f r o m M e t z G o r g e is s im p l y a r e f le c t i o n o f i ts v e r y u n u s u a l y e a s t c o m -

p o s i t i o n ( T a b l e 3 ). T h e h i g h f r e q u e n c y o f K .

apicu la ta

m a i n t a i n e d t h e g e n er a ll y

l o w r e s o u r c e u t i l i z a t i o n c h a r a c t e r i s t i c t y p i c a l o f c a c t u s y e a s t f lo r a e [1 0 ], b u t a

l a r g e p r o p o r t i o n o f Cr . i n f i rm o-m i n i a t us i n t h i s c o m m u n i t y g a v e i t a u n i q u e

p r o f i l e w i t h r e s p e c t to t r a i ts t h a t a r e s p ec if ic t o t h a t y e a s t a n d t o b a s i d i o m y c e t o u s

y e a s t s i n g e n e r a l .

i s c u s s i o n

I t is c l e a r f r o m t h e a n a l y s is o f t h e d a t a ( T a b l e 5 ) t h a t y e a s t c o m m u n i t i e s o f

c l a d o d e s a n d f ru i ts a re d i s t in c t , a n d y e t s o m e o v e r l a p d o e s o c c u r . E a r l ie r a n a l -

y s e s o f D rosoph i l a h a b i t a t s h a d i n d i c a t e d t h a t O p u n t i a c l a d o d e y e a s t c o m -

m u n i t i e s w e r e m o r e s i m i l a r t o y e a s t c o m m u n i t i e s o f c o l u m n a r c a ct i [ 14 ] t h a n

t o t h o s e f r o m f r u i t s . H o w e v e r , t h e f r u i t s s t u d i e d w e r e n o t c a c t u s f r u i t s a n d

c o u l d h a v e b e e n d i s t i n c t f o r o t h e r r e a s o n s . I t i s n o w a p p a r e n t t h a t t h e c a c t u s

f ru i t y e a s t c o m m u n i t y , e v e n w h e n t h e f ru i ts a r e p h y s ic a l ly n e x t to t h e c l a d o d e

h a b i t a t , i s q u a n t i t a t i v e l y a n d q u a l i t a t i v e l y d i f fe r e n t f r o m t h e c l a d o d e y e a s t

c o m m u n i t y . T h e r e a s o n s f o r t h e d i f fe r e n c e a r e n o t e n t i r e l y c l ea r , a l t h o u g h i t is

p r e s u m a b l y b a s e d o n t h e c h e m i c a l n a t u r e o f t h e t w o s u b s t r a te s . A l l o f t h e y e a s ts

r e c o v e r e d f r o m t h e t w o s u b s t r a te s c a n g r o w o n e i t h e r f r u i t o r c l a d o d e t i ss u e

w h e n i n o c u l a t e d o n t h e m . T h e c o m m u n i t y d i f fe r en c e is t h u s n o t a c h e m i c a l

i n h i b i t o r p r e s e n t i n t h e d i f f e re n t t is s u es . S p e c i es - s p ec i e s in t e r a c t i o n s m a y b e

i m p o r t a n t i n t h a t f r u i t y e a s ts t e n d t o c a r r y k i l l e r f a c t o r s m o r e o f t e n t h a n

c l a d o d e y e a s t s . A l l o f t h e i s o l a t e s ( T a b l e s 2 - 3 ) w e r e t e s t e d f o r k i l le r a c t i v i t y

a g a i n s t a s t a n d a r d s e n s i t i v e s t r a i n C. g labrata Y 5 5 ) , a n d t h e f o l l o w i n g s p e ci e s

t e s t e d p o s i t i v e f o r k i l l e r a c t i v i t y : ( 1 ) P. kluyverL a l l s t r a i n s ; ( 2 ) K. apiculata,

m o s t s t r a i n s ; ( 3 ) P. opunt iae, a ll s tr a in s f r o m l o c a l it y # 1 3 ( H e m m a n t ) b u t n o t

e l s e w h e r e ; ( 4 )

H. cal i fornica,

f r o m l o c a l i t y # 1 1.

I t i s t h e r e f o r e p o s s i b l e t h a t c o m m u n i t y s t r u c t u r e o f t h e f r u i t h a b i t a t i s p a r t ia l l y

d e t e r m i n e d b y k i l le r a c t i v i t y o f t h e r e s i d e n t y e a s ts . T h i s is f ea s ib l e b e c a u s e t h e

l o w p H o f f r u i t ( p H = 3 - 4 ) c o i n c i d e s w i t h t h e o p t i m u m p H f o r k i l l e r t o x i n [ 7].

H o w e v e r , w e h a v e n o t s y s t em a t i c a l l y te s te d r e s is t a n c e / s e n s i t i v i t y p a t t e r n s o f

y e a s t s r e s t r i c t e d t o t h e c l a d o d e h a b i t a t ( i .e .,

Cr. cereanus

c o m p l e x a n d

P. opun-

t iae) t o t h e c o m m o n k i ll e r f ru i t y e a s t K. apicu la ta a n d t o P. kluyveri w h i c h


13/14

Com parison of Yeast Com mu nities in Necrotic Tissue 191

l iv e s i n b o t h h a b i t a t s . F u r t h e r m o r e , t h e p H o f c l a d o d e r o t s r a p i d l y r is es f r o m

a b o u t 4 t o 8 - 9 w h e r e t h e k i l le r t o x i n s a r e i n e f fe c t i v e .

I t i s n o t s u r p r i s in g t h a t t h e c l a d o d e c o m m u n i t i e s o f t h e t w o r e g i o n s a re

s i m i la r , e s p e c ia l ly b e c a u s e o f t h e i n t r o d u c t i o n i n to A u s t r a l ia o f c la d o d e m i -

c r o b i o t a i n s u c h l ar g e a m o u n t s d u r i n g t h e b i o lo g i c a l c o n t r o l p r o g r a m . T h e

d i f f e re n c e s b e t w e e n t h e r e g i o n s f o r y e a s t c o m m u n i t i e s o f f ru i t s, h o w e v e r , c o u l d

b e b a s e d o n t h e e x t r i n s i c m i c r o b i o t a , i .e ., y e a s t c o m m u n i t y o f o t h e r f r u it s a n d

t h e i r y ea s t c o m m u n i t i e s r e s id e n t i n A u s t r a l ia . P r e s u m a b l y m o s t , i f n o t a l l , o f

t h e r o t t i n g m a t e r i a l s a n d c u t p o r t i o n s o f p r i c k ly p e a r [8] s h i p p e d t o A u s t r a l i a

f o r t h e b i o l o g i ca l c o n t r o l p r o g r a m w e r e c l a d o d e s a n d n o t f r u it .

I n a d d i t i o n , o t h e r n o n c a c t u s b r e e d i n g d r o s o p h i l i d s a s w e l l a s b e e s , w a s p s ,

a n d o t h e r i n s e c ts a r e f e e d i n g a n d / o r b r e e d i n g i n th e O . stricta f r u i t , t h u s p r o -

v i d i n g a v e c t o r i n g p a s s a g e f o r e x t r i n s ic m i c r o o r g a n i s m s . E v e n b i r d s f e e d in g o n

c a c t u s f ru i t c o u l d i n t r o d u c e y e a s t s f r o m o t h e r f r u i t w h e r e p r e s e n t . T h i s i s n o t

t h e c a s e fo r t h e c l a d o d e s b e c a u s e Drosophila buzzatii a n d D. aldrichi i n t r o d u c e d

d u r i n g b i o l o g i c a l c o n t r o l e f f o r t s , a r e b o t h r e s t r i c t e d t o b r e e d i n g i n c l a d o d e s ,

a n d a p p a r e n t l y h a v e e x c l u s i v e u s e a m o n g t h e d r o s o p h i l i d s o f t h is h a b i t a t [ 1].

I n t h i s s e n s e t h e cactus-microorganism-Drosophila s y s t e m i s c l o s e d w i t h r e s p e c t

t o t h e c l a d o d e s b u t u n c o u p l e d a n d o p e n w i t h r e s p e c t t o t h e f ru i ts . T h i s s u p -

p o s i t i o n i s r e i n f o r c e d b y t h e s e a s o n a l n a t u r e o f f r u i t p r o d u c t i o n , w h i c h c a u s e s

a h i a t u s e v e r y y e a r in t h e c o n t i n u a t io n o f r o t - t o - r o t c o m m u n i t y d y n a m i c s .

I n t e r m s o f o v e r a l l p h y s i o lo g i c a l s p ec if ic i t y , t h e c l a d o d e y e a s t c o m m u n i t i e s

d e s c r i b e d i n th i s s tu d y w e r e r a t h e r t y p i c a l o f o t h e r c a c t o p h i l i c y e a s t c o m m u -

n i t i e s. T h e a n a l y s i s o f 67 9 c a c t o p h i l i c y e a s t s t r a i n s ( o r is o la t es ) b y t h e s a m e

m e t h o d [1 0] h a d s h o w n c l ea r ly t h a t th e y d i f fe r f r o m r a n d o m y e a s t a s s e m b l a g e s

b y t h e i r v e r y h i g h d e g r e e o f n u t r i t i o n a l s p e c i a l iz a t i o n , g i v i n g h i g h e r t h a n e x -

p e c t e d r e s p o n s e s f o r g r o w t h o n p r i m a r y a l c o h o l s a n d o r g a n i c ac id s , a n d o f

c o u r s e , f o r g r o w t h a t 3 7~ A t v a r i a n c e w i t h th e re s u l ts f o u n d p r e v i o u s l y [ 10 ],

s i g n if i ca n t ly h i g h f e r m e n t a t i v e a b i l i t i e s p r e v a i l e d i n a l m o s t h a l f t h e c o l l e c t io n s

a n a l y z e d h e r e . I n t e r e s t i n g l y , m o s t c o l l e c t i o n s e x h i b i t i n g t h i s s p e c i a l f e a t u r e

w e r e f r o m A u s t r a l i a n s it es .

Acknowledgments.

Support for this research was provided by the National Science Foundation

Gra nts DEB 81-08679 (WTS), DEB 81-08898 HJP), IN T 83-17743 (WTS); by an operating grant

of the N atural Science and E ngineering Research Council o f Ca nada (MAL); and by the University

of New England Visiting Fellowship Program (WTS). We are grateful for the cooperation and

helpful discussions with J. S. F. Barker, J. C. Fogleman, an d W . B. Heed.

e f e r e n c e s

1. B arker JSF 1982) Population gen etics o f Opuntiabreeding Drosophilain Australia. In: Barker

JSF, Starmer W T (eds) Ecological genetics an d ev olution: the

cactus-yeast-Drosophila

model

system. Academic Press, Sydney, Australia, pp 209-224

2. Barker JSF, Mu lley JC (1976) Isozy m e varia tion in natural populations

of Drosophila buzzatiL

Evolution 30:213-233

3. Barker JSF, Toll GL , East PD, M iranda M , Phaf f H J (1983) Heterogeneity of the yeast flora

in the breeding sites ofcactophilic Drosophila.Can J Microbioi 29:6-14

4. Barker JSF, East PD, Ph affH J, M iranda M (1984) The ecology of the yeast flora in necrotic

Opuntia

cacti and o f associated

Drosophila

in Australia. Microb Ecol 10:379-399


14/14

1 92 W . T . S t a r m e r e t a l.

5 . Ba r n e t t J S , P a y n e R W , Ya r r o w D 1 9 8 3 ) Ye a s t s : c h a r a c t e r i s ti c s a n d i d e n t i f i c a t io n . Ca m b r id g e

U n i v e r s i t y P re ss , C a m b r i d g e , U n i t e d K i n g d o m

6 . B e n s o n L 1 9 8 2) T h e c a c t i o f th e U n i t e d S t a t e s a n d C a n a d a . S t a n f o r d U n i v e r s i t y P r es s,

S t a n f o r d , Ca l i f o r n i a

7 . Bu s s e y H 1 9 8 1 ) P h y s io lo g y o f k i l l e r f a c to r i n y e a s t. Ad v M ic r o b i a l P h y s io l 2 2 :9 3 - 1 2 2

8 . D o d d A P 1 9 4 0) T h e b i o lo g i c a l c a m p a i g n a g ai n s t p r i c kl y - p e ar . G o v e r n m e n t P r i n te r , B r i sb a n e ,

Q u e e n s l a n d , A u s t r a li a

9 . G a r c i a T u d u r i J C , M a r t o r e l l L F , M e d i n a G a u d S 1 9 7 1) G e o g r a p h i c a l d i s t r i b u t i o n a n d h o s t

p l a n ts o f t h e c a c t us m o t h Cactoblastis cactorum B e rg ) i n P u e r t o R i c o a n d t h e U n i t e d S t a te s

V i r g i n I s l a n d s . J A g r U n i v P u e r t o R i c o 5 5 : 1 3 0 - 1 3 4

1 0. L a c h a n c e M A , S t a r m e r W T 1 9 86 ) T h e c o m m u n i t y c o n c e p t a n d t h e p r o b le m o f n o n - t r iv i a l

c h a r a c t e r iz a t i o n o f y e a s t c o m m u n i t i e s . C o e n o s e s 1 : 2 1 - 28

1 1. M c F a y d e n R E I 9 8 5 ) L a r v a l c h ar a c t er i st i c s o f Cactoblastis s p p . L e p id o p t e r a : P y r a l i d a e ) a n d

th e s e l e c t i o n o f s p e c i es f o r b io lo g i c a l c o n t r o l o f p r ic k ly p e a r s Opuntia spp . ) . Bu l l En t Res 75 :

1 5 9 - 1 6 8

1 2. M u r r a y N D 1 9 8 2 ) E c o l o g y a n d e v o l u t i o n o f t h e

Opuntia-Cactoblastis

e c o s y s t e m in Au s t r a l ia .

I n : Ba r k e r J S F , S t a r r n e r W T e d s) E c o lo g i c a l g e n e t i c s a n d e v o lu t i o n : t h e cactus-yeast-Dro-

sophila m o d e l s y s t e m . A c a d e m i c P re s s, S y d n e y , A u s t r a l ia , p p 1 7 - 3 0

1 3. S i m m o n d s F J , B e n n e t t F D 1 9 66 ) B i ol o g ic a l c o n t r o l o f Opuntia s p p . b y Cactoblastis cactorum

i n t h e L e e w a r d I s la n d s W e s t I n d ie s ). E n t o m o p h a g a 1 1 : 1 8 3 - 1 8 9

1 4. S t a r m e r W T 1 9 8 1) A c o m p a r i s o n o f

Drosophila

h a b i t a t s a c c o r d in g t o t h e p h y s io lo g i c a l a t -

t r ib u t e s o f th e a s s o c i a t ed y e a s t c o m m u n i t i e s . E v o l u t i o n 3 5 : 3 8 - 5 2

1 5. S t a r m e r W T , P h a f f H J 1 9 8 3 ) A n a l y s i s o f t h e c o m m u n i t y s t r u c tu r e o f y e a s t s a s s o c i a te d w i t h

t h e d e c a y i n g s t e m s o f c a c tu s I I . Opuntia s p e c i e s . M ic r o b E c o l 9 :2 4 7 - 2 5 9

1 6. V a n d e r W a l t J P 1 9 7 0 ) Cr i t e r i a a n d m e th o d s u s e d in c l a s s if i c a ti o n . I n : L o d d e r J e d ) T h e

y e a s t s , a t a x o n o m i c s t u d y . N o r t h H o l l a n d , A m s t e r d a m , p p 3 4 - 1 1 3

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A Comparison of Yeast Communities Found in Necrotic Tissue of Cladodes and Fruits of Opuntia