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The relationship between the production of hypogeous sporocarps and the denisity and diet of northern… Anderson, Janice 2003

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THE RELATIONSHIP BETWEEN THE PRODUCTION OF H Y P O G E O U S S P O R O C A R P S A N D T H E D E N S I T Y A N D DIET O F N O R T H E R N F L Y I N G S Q U I R R E L S IN W E S T E R N H E M L O C K F O R E S T S O F C O A S T A L BRITISH C O L U M B I A by JANICE ANDERSON B . S c . (Animal Biology), T h e University of British C o l u m b i a , 1994  A T H E S I S S U B M I T T E D IN P A R T I A L F U L F I L L M E N T O F THE REQUIREMENTS FOR THE D E G R E E OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE STUDIES (Department of Forest S c i e n c e s )  W e a c c e p t this thesis a s conforming to the required standard  T H E UNIVERSITY O F BRITISH C O L U M B I A  December 2003 © J a n i c e Anderson, 2003  Library Authorization  In presenting this thesis in partial fulfillment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission.  Janice Anderson  17/12/2003  Name of Author (please print)  Date (dd/mm/yyyy)  Title of Thesis:  T H E RELATIONSHIP B E T W E E N T H E P R O D U C T I O N O F  H Y P O G E O U S S P O R O C A R P S A N D T H E DENSITY A N D DIET O F N O R T H E R N FLYING S Q U I R R E L S IN W E S T E R N H E M L O C K F O R E S T S O F C O A S T A L BRITISH C O L U M B I A Degree:  M.Sc.  Department of  Year: Forest Sciences  The University of British Columbia Vancouver, B C Canada  2003  II  ABSTRACT  T h e northern flying squirrel, Glaucomys sabrinus (Shaw), is a n arboreal sciurid inhabiting forested habitats a c r o s s North A m e r i c a . H y p o g e o u s fruit b o d i e s of mycorrhizal fungi (truffles) are a predominant food e a t e n by northern flying squirrels. P r e v i o u s studies h a v e s u g g e s t e d that the a b u n d a n c e of truffles in a stand m a y be a n important factor a s s o c i a t e d with the density of northern flying squirrels. O v e r a twoy e a r period, five s e c o n d - g r o w t h w e s t e r n h e m l o c k (Tsuga heterophylla (Raf). Sarg.) forests in c o a s t a l British C o l u m b i a w e r e u s e d year-round to s a m p l e truffles a n d to live trap northern flying squirrels, in order to: (1) d e s c r i b e the o c c u r r e n c e a n d production of truffles; (2) determine the importance of truffles in the s e a s o n a l diet of squirrels; (3) identify which truffle taxa w e r e selectively c o n s u m e d by this s p e c i e s ; a n d 4) evaluate a s s o c i a t i o n s b e t w e e n the density of northern flying squirrels a n d the production of truffles. Truffle production from e a c h site w a s determined using results from the primary collection period, w h i c h included four s a m p l e s at 10-week intervals from April 1998 to D e c e m b e r 1998. E l e v e n s p e c i e s representing six g e n e r a of truffles w e r e collected, with Elaphomyces m a k i n g up o v e r 9 3 % of the total n u m b e r a n d 9 9 % of the total b i o m a s s . Truffle production at e a c h site during the primary collection period ranged from 1.68 kg ha" year" to 15.72 kg h a " year" . Plant material w a s a major year-round c o m p o n e n t of the diet of northern flying squirrels, suggesting a more generalist feeding strategy than reported e l s e w h e r e . Truffle s p o r e s w e r e m o s t frequent in the s u m m e r a n d fall diets. N i n e additional truffle taxa w e r e present in squirrel diets than w e r e collected in the field. Northern flying squirrels c o n s u m e d on a v e r a g e 1.9 times more truffle t a x a than w e r e found during concurrent fungal s u r v e y s . T h e fungi g e n e r a Elaphomyces a n d Hydnotrya were under-represented a n d s e v e r a l t a x a w e r e over-represented in squirrel f e c e s relative to their a b u n d a n c e at the site. Densities of flying squirrels c o u l d not be e x p l a i n e d by truffle production a l o n e at the five sites. Efforts to e n h a n c e populations of northern flying squirrels to improve foraging habitat for the e n d a n g e r e d northern spotted owl (Strix occidentalis caurina Merriam) s h o u l d c o n s i d e r m e a s u r e s that affect a broad array of food items a n d that e n h a n c e diversity a s well a s a b u n d a n c e of food supply. 1  1  1  1  Key Words: northern flying squirrel, h y p o g e o u s fungi, truffles, m y c o p h a g y , northern spotted owl, food limitation, fecal s a m p l e s .  in TABLE OF CONTENTS  ABSTRACT  ii  TABLE OF CONTENTS  iii  LIST O F T A B L E S  iv  LIST O F F I G U R E S  vi  ACKNOWLEDGEMENTS INTRODUCTION Rationale Literature R e v i e w Objectives  viii 1 1 3 30  MATERIALS AND METHODS  33  RESULTS  54  DISCUSSION  79  C O N C L U S I O N S A N D M A N A G E M E N T IMPLICATIONS  90  LITERATURE CITED  92  APPENDIX 1 107 Truffle g e n e r a a n d type found at e a c h site during o n e to 4 s e s s i o n s from M a y 1997 to F e b r u a r y 1998 a n d o n e c a n c e l e d s e s s i o n in F e b r u a r y 1999. APPENDIX 2 108 T h e o c c u r r e n c e of e a c h g e n u s of truffle in the diet of northern flying squirrels (shaded) a n d found during truffle s e s s i o n s (x) at the five study sites.  iv  LIST O F T A B L E S Page  T a b l e 1.  S u m m a r y of studies describing the diet of northern flying squirrels in the wild. V a l u e s are s u m m a r i z e d or reported directly from tables, estimated from g r a p h s , or obtained from information in the text 7  T a b l e 2.  T h e apparent digestibility of fungi c o n s u m e d by m y c o p h a g i s t s during feeding trials a n d their digestive strategies 19  T a b l e 3.  S u m m a r y of the n u m b e r of taxa, density, a n d standing crop of truffles collected in published studies from the P a c i f i c Northwest. V a l u e s are taken directly from, c a l c u l a t e d from, or e s t i m a t e d (~) using tables or g r a p h s in the citation 26  T a b l e 4.  M e a n density (trees/ha) ± S E of the four m a i n tree s p e c i e s a n d all tree s p e c i e s at the five sites (N=20) 36  T a b l e 5.  M e a n d i a m e t e r s at breast height (cm) ± S E of the four m a i n tree s p e c i e s a n d all tree s p e c i e s at the five sites (N=20) 36  T a b l e 6.  Truffle s a m p l i n g s c h e d u l e at the five sites during the four s e s s i o n s in 1997 a n d early 1998, prior to i m p r o v e m e n t s in the s a m p l i n g methodology 39  T a b l e 7.  Truffle s a m p l i n g s c h e d u l e at the five sites during the primary collection period in 1998 a n d 1 c a n c e l e d s e s s i o n in 1999, following i m p r o v e m e n t s in the s a m p l i n g methodology 40  T a b l e 8.  S u m m a r y of m e t h o d s u s e d to s a m p l e truffle populations in p u b l i s h e d studies from the P a c i f i c Northwest during the past 30 y e a r s 42  T a b l e 9.  Truffle s p e c i e s a n d type found at e a c h site during the primary collection period 55  T a b l e 10.  Truffle s p e c i e s found at the five sites during e a c h s e s s i o n in the primary collection period 56  T a b l e 11.  N u m b e r s a n d b i o m a s s (g dry weight) of truffle s p e c i e s found within 6 2 6 plots s a m p l e d during the primary collection period at the five sites 57  T a b l e 12.  P e r c e n t a g e of plots with at least o n e truffle collected during e a c h s e s s i o n at the five sites both a) prior to a n d b) following c h a n g e s in the s a m p l i n g m e t h o d s . V a l u e s in p a r e n t h e s e s are the n u m b e r of 4 - m plots s a m p l e d per s e s s i o n 58  3  2  V  T a b l e 13.  S u m m a r y of the v a l u e s from the habitat survey u s e d to determine correction factors for standardizing truffle production o n a per hectare basis 60  T a b l e 14.  Indices of truffle production for e a c h site b a s e d on standing c r o p s from the primary collection period 60  T a b l e 15.  N u m b e r of fecal s a m p l e s e x a m i n e d within e a c h s e a s o n collected from northern flying squirrels during two y e a r s of live-trapping at five sites...61  T a b l e 16.  Major food i t e m s by s e a s o n that w e r e o b s e r v e d in f e c a l s a m p l e s collected from resident northern flying squirrels at the five sites b e t w e e n J a n u a r y 1997 a n d D e c e m b e r 1998 64  T a b l e 17.  T h e n u m b e r of truffle taxa found during truffle s e s s i o n s (S) a n d in the diet (D) of northern flying squirrels 65  T a b l e 18.  M e a n estimated population s i z e from mark-recapture of northern flying squirrels during e a c h s e a s o n in over two y e a r s of live trapping 75  T a b l e 19.  M e a n estimated Jolly trappability of northern flying squirrels live-trapped at five sites during e a c h s e a s o n 76  Table 20.  M e a n squirrel m o v e m e n t , effective trapping squirrel density  b  a r e a , a n d e s t i m a t e s of 77  VI  LIST O F F I G U R E S Page Figure 1.  Location of five study sites s a m p l e d for truffles a n d northern squirrels in 1997 and 1998  Figure 2.  T h e corrected standing crop of truffles collected on e a c h site during the primary collection period a n d early 1999, s t a n d a r d i z e d to b i o m a s s per hectare (A) and n u m b e r per hectare (B). S a m p l i n g effort w a s consistent for the first four s e s s i o n s ; only two sites w e r e s a m p l e d in winter 1999 59  Figure 3.  T h e p e r c e n t a g e of f e c a l s a m p l e s within e a c h s e a s o n that contained 'major' food items (i.e. occurred in at least 5 % of the 7 5 fields e x a m i n e d per s a m p l e ) . T h e n u m b e r of f e c a l s a m p l e s e x a m i n e d during e a c h s e a s o n is given in p a r e n t h e s e s 62  Figure 4.  T h e standing crop of truffle taxa found at C a p i l a n o a n d the f r e q u e n c y of truffle taxa in the diet (i.e. % of fecal s a m p l e s containing e a c h truffle t a x a a s a major food item) during concurrent (within 5 w e e k s ) s a m p l i n g . N u m b e r of fecal s a m p l e s e x a m i n e d : N = 3 (D), N = 5 (A, B, C ) 68  Figure 5.  T h e standing crop of truffle taxa found at C h e h a l i s a n d the f r e q u e n c y of truffle t a x a in the diet (i.e. % of fecal s a m p l e s containing e a c h truffle taxa a s a major food item) during concurrent (within 5 w e e k s ) s a m p l i n g . N u m b e r of f e c a l s a m p l e s e x a m i n e d : N = 3 (C), N = 4 (B), N = 5 (A, D) 69  Figure 6.  T h e standing crop of truffle taxa found at C o q u i t l a m a n d the f r e q u e n c y of truffle t a x a in the diet (i.e. % of f e c a l s a m p l e s containing e a c h truffle taxa a s a major food item) during concurrent (within 5 w e e k s ) s a m p l i n g . N u m b e r of f e c a l s a m p l e s e x a m i n e d : N = 4 (A), N = 5 (C), N = 7 (D), N = 9(B) 70  Figure 7.  T h e standing crop of truffle taxa found at the R e s e a r c h Forest a n d the f r e q u e n c y of truffle taxa in the diet (i.e. % of f e c a l s a m p l e s containing e a c h truffle taxa a s a major food item) during concurrent (within 5 w e e k s ) s a m p l i n g . N u m b e r of f e c a l s a m p l e s e x a m i n e d : N = 1 (A, E ) , N = 3 ( D ) , N = 5 ( B , C) 71  Figure 8.  T h e standing crop of truffle taxa found at the S e y m o u r Demonstration Forest a n d the f r e q u e n c y of truffle taxa in the diet (i.e. % of f e c a l s a m p l e s containing e a c h truffle taxa a s a major food item) during concurrent (within 5 w e e k s ) s a m p l i n g . N u m b e r of f e c a l s a m p l e s e x a m i n e d : N = 6 (B, C ) , N = 13 (A) 72  Figure 9.  E s t i m a t e d population s i z e of resident trapped at the five sites for 36 months  northern  flying  squirrels  flying 34  live74  Vll  Figure 10. T h e relationship b e t w e e n the a b u n d a n c e a n d o c c u r r e n c e of truffles a n d the density of northern flying squirrels at e a c h site. Correlation coefficients are p r e s e n t e d on e a c h graph for two s c e n a r i o s : including C A P (r ) a n d excluding C A P (/) 78 a  Vlll  ACKNOWLEDGEMENTS I would like to express my gratitude to my research supervisor, Dr. Dan Durall, for his guidance, enthusiastic support, and constant throughout my research.  encouragement  I am grateful to my academic supervisor, Dr. Cindy  Prescott, for handling administrative matters and providing helpful advice during my program.  I would like to thank all of my committee members, including Dr. Karl  Larsen, Dr. Peter Marshall, Dr. Prescott, and Dr. Durall, for their ready assistance and helpful comments on earlier versions of the thesis. I am deeply indebted to the following people for their hard work and dedication in the field: B. Anderson, F. Moreau, N. Handford, T. Burke, S. Taylor, and Dr. Doug Ransome. I express my appreciation to the numerous volunteers who assisted with collecting truffles, especially B. Anderson, R. Alden, T. Nivens, M. Culham, Y. Huang, C. Carpenter, and G. Robertson. I would like to thank Dr. Efren Cazares and Dr. Michael Castellano for providing training in truffle identification and fecal pellet analysis and supplying voucher specimens for reference.  Dr. Cazares  provided assistance with identification of unknown structures and spores in the fecal samples. My thanks to Dr. Durall for providing laboratory facilities and equipment used in the study. I extend my thanks to J. Hobbs for his help with the map used in Figure 1.  D. Bonin (GVRD Watershed Management) supplied access to the  Capilano and Coquitlam watersheds.  I am also indebted to Dr. Ransome for his  assistance, encouragement, and thought-provoking discussions. I am grateful to Dr. Tom Sullivan and Dr. Ransome for obtaining the necessary funds from the following agencies, organizations, and companies to support this research: B.C. Ministry of Forests (Kamloops Region), Ministry of  ix Environment,  Lands and  Parks,  National S c i e n c e s a n d  Engineering R e s e a r c h  C o u n c i l , Forest R e n e w a l British C o l u m b i a , Forestry C a n a d a , S c i e n c e C o u n c i l of British C o l u m b i a , C a n a d i a n Forest P r o d u c t s Ltd., International Forest P r o d u c t s Ltd., J . S . J o n e s T i m b e r Ltd., T e r m i n a l F o r e s t P r o d u c t s Ltd., C a t t e r m o l e T i m b e r Ltd., Pretty's T i m b e r C o m p a n y Ltd., a n d H e r m a n S a w m i l l s Ltd.  A s the recipient of the  N a m k o o n g F a m i l y F e l l o w s h i p in Forest S c i e n c e s for two y e a r s , I e x p r e s s my appreciation to the N a m k o o n g family for this financial support. Finally, I a m d e e p l y grateful to my friends a n d family for their  continual  r e a s s u r a n c e a n d support a n d for helping m e s e e my w a y to the e n d of this p r o g r a m . T h a n k y o u B r e n d a n for your patience, g o o d h u m o u r a n d e n c o u r a g e m e n t , although this w a s a long journey you m a d e every step of the w a y enjoyable.  1  INTRODUCTION  RATIONALE In 1 9 8 6 , the C o m m i t t e e o n the Status of E n d a n g e r e d Wildlife in C a n a d a (COSEWIC)  designated  the northern  Merriam) a s nationally Endangered  spotted  owl (Strix  (Dunbar et al. 1991).  occidentalis  caurina  T h i s designation w a s  reconfirmed in 2 0 0 0 in r e s p o n s e to reports highlighting e x t e n s i v e a n d continuing l o s s , isolation, a n d fragmentation of late s u c c e s s i o n a l forested habitat in c o a s t a l British C o l u m b i a a n d the low a n d declining owl a b u n d a n c e within t h e s e a r e a s (Dunbar a n d B l a c k b u r n 1 9 9 4 ; C O S E W I C 2000). species  c o u p l e d with this  owl's  C o n s e r v a t i o n c o n c e r n for this  a s s o c i a t i o n with  old-growth  stands  of  high  c o m m e r c i a l v a l u e h a v e g e n e r a t e d m u c h interest a n d r e s e a r c h o n the northern spotted owl throughout its range in the Pacific Northwest ( F o r s m a n et al. 1 9 8 4 ; T h o m a s er al. 1 9 9 0 ; G u t i e r r e z et al. 1995). T h e selection (e.g. F o r s m a n et al. 1 9 8 9 ; C a r e y et al. 1 9 9 2 ; Mills er al. 1 9 9 3 ; S w i n d l e et al. 1999), spatial a r r a n g e m e n t (e.g. T h o m a s et al. 1 9 9 0 ; C a r e y et al. 1992, 1994), a n d a m o u n t (e.g. F o r s m a n etal. 1984; C a r e y etal. 1 9 9 0 , 1992) of o l d growth forest u s e d by breeding pairs of spotted owls h a v e b e e n investigated in m a n y studies.  In addition  highlighted  to identifying  habitat  requirements,  Carey  et al.  (1992)  the importance of understanding the e c o l o g y of the owl's prey in  d e v e l o p i n g effective m a n a g e m e n t plans for the spotted o w l .  Differences in prey  b i o m a s s e x p l a i n e d the s t a n d s s e l e c t e d a n d the a r e a s of old forest u s e d annually by foraging pairs of northern spotted owls in W a s h i n g t o n a n d O r e g o n ( C a r e y et al. 1992).  T h e a b u n d a n c e a n d type of prey w e r e better predictors of the h o m e range  s i z e of northern spotted owls than w a s the proportion of older forests in California  2 a n d O r e g o n (Zabel et al. 1995).  Differences in prey a b u n d a n c e a n d distribution  affected the selection of habitats u s e d by foraging northern spotted owls in California (Zabel et al.  1995; W a r d et al.  1998).  N o o n a n d Biles (1990) s u g g e s t that  silvicultural prescriptions that i n c r e a s e owl's foraging s u c c e s s are the most likely w a y to i n c r e a s e the population growth rate of spotted owls. T h e northern flying squirrel (Glaucomys  sabrinus  S h a w ) is a major prey of the  northern spotted owl through the owl's northern range ( F o r s m a n et al. 1984, 1 9 9 1 ; T h o m a s et al. 1990; C a r e y 1 9 9 1 ; C a r e y et al. 1992; C a r e y 1993).  Flying squirrels  represent 4 7 to 6 1 % of the b i o m a s s of prey in diets of spotted owls from c o a s t a l British C o l u m b i a ( B . C . ) (Dunbar a n d B l a c k b u r n 1994) a n d W a s h i n g t o n ( F o r s m a n et al. 1 9 9 1 ; C a r e y 1993).  T h u s , understanding differences in the density of northern  flying squirrels a m o n g habitats h a s b e e n the f o c u s of m u c h recent r e s e a r c h (e.g. R a n s o m e a n d Sullivan 1997, 2 0 0 2 , 2 0 0 3 , 2 0 0 4 ; C a r e y etal. 1999, 2 0 0 0 a , 2001). P r e v i o u s studies have investigated h o w stand a g e (Volts 1986; C a r e y 1 9 9 1 , 1995; C a r e y et al. 1992, 1999; Witt 1992; W a t e r s a n d Z a b e l 1995) a n d structural attributes ( R o s e n b e r g a n d A n t h o n y 1992; W a t e r s a n d Z a b e l 1995; C a r e y 1995; C a r e y et al. 1999) affect densities of flying squirrels, but with inconsistent results. S o m e studies h a v e s u g g e s t e d that the a b u n d a n c e of their primary food is a n important factor determining the density of northern flying squirrels ( R o s e n b e r g a n d A n t h o n y 1992; W a t e r s a n d Z a b e l 1995; R a n s o m e a n d Sullivan 1997). (underground fruitbodies of h y p o g e o u s fungi described  Truffles  below) are a predominant  food of northern flying squirrels in the P a c i f i c Northwest (Table 1).  Although a  n u m b e r of r e s e a r c h e r s have experimentally manipulated food r e s o u r c e s for s m a l l m a m m a l populations using 'artificial' food (i.e. sunflower s e e d s Helianthus  annuus)  (Sullivan 1990; Sullivan a n d Sullivan 1982; Sullivan et al. 1983; K l e n n e r a n d K r e b s  3 1 9 9 1 ; R a n s o m e a n d S u l l i v a n 1997), no previous r e s e a r c h h a s a d d r e s s e d the role of natural food r e s o u r c e s , s u c h a s the a b u n d a n c e of truffles, in limiting populations of northern flying squirrels. T h i s study investigates the relationship b e t w e e n northern flying squirrels a n d truffles within five s e c o n d - g r o w t h coniferous s t a n d s in c o a s t a l B . C . , a s part of a larger project e x a m i n i n g r e s o u r c e limitations a n d  population  d y n a m i c s of northern flying squirrels ( R a n s o m e a n d Sullivan 2 0 0 2 , 2 0 0 3 , 2004). T h e intent is to improve our understanding of the e c o l o g y of northern flying squirrels in c o a s t a l B . C . a n d s u b s e q u e n t l y aid in the m a n a g e m e n t of the e n d a n g e r e d northern spotted owl.  LITERATURE REVIEW  The Northern Flying Squirrel T h e northern flying squirrel is widely distributed in forested regions a c r o s s northern North A m e r i c a ( W e l l s - G o s l i n g a n d H e a n e y 1984). In the P a c i f i c Northwest, northern flying squirrels inhabit a variety of w o o d l a n d habitats from c o a s t a l B . C . , through the C a s c a d e R a n g e of W a s h i n g t o n a n d O r e g o n a n d into California ( W e l l s G o s l i n g a n d H e a n e y 1984; M a s e r et al. 1985). Flying squirrels h a v e b e e n f o u n d in s t a n d s of conifers (e.g. M c K e e v e r 1960; G r o d z i n s k i 1 9 7 1 ; M a s e r et al. 1 9 7 8 a , 1978b,  1981;  Ransome  and  Sullivan  1997),  mixed  conifer-hardwoods  (e.g.  M a c D o n a l d 1996; C u r r a h etal. 2000) a n d pure h a r d w o o d s (e.g. W e i g l 1978; W e l l s G o s l i n g a n d H e a n e y 1984). T h e northern flying squirrel is a n arboreal m e m b e r of the family S c i u r i d a e in the order R o d e n t i a . T h i s nocturnal s p e c i e s generally exhibits a single bout (Mowrey  4 a n d Z a s a d a 1984; Cotton a n d P a r k e r 2 0 0 0 a ) or a b i p h a s i c pattern of activity for a few hours after d u s k a n d again before d a w n (Weigl a n d O s g o o d 1974; W e l l s G o s l i n g a n d H e a n e y 1984; Witt 1992; Cotton a n d P a r k e r 2 0 0 0 a ) . D e n sites u s e d by northern flying squirrels are regularly c h a n g e d (Mowrey a n d Z a s a d a 1984; every two w e e k s on a v e r a g e , C a r e y et al. 1997; Cotton a n d P a r k e r 2 0 0 0 b ) a n d include both constructed nests a n d cavities in trees ( C o w a n 1936; W e i g l a n d O s g o o d 1974; W e i g l 1978; M o w r e y a n d Z a s a d a 1984; C a r e y et al. 1997). Northern flying squirrels d o not a p p e a r to b e territorial; they d o not display territorial v o c a l i z a t i o n s ( W e l l s G o s l i n g a n d H e a n e y 1994) or d e f e n s e w h e n interacting with c o n s p e c i f i c s in captivity (Weigl 1978) or in the field ( C a r e y 1991) a n d they are not known to a c c u m u l a t e or d e f e n d food c a c h e s ( W e l l s - G o s l i n g a n d H e a n e y 1984).  Furthermore, this s p e c i e s  u s e s c o m m u n a l d e n s ( M a s e r et al. 1 9 8 1 ; M o w r e y a n d Z a s a d a 1984; C a r e y et al. 1997; F e e n 1997; Cotton a n d P a r k e r 2 0 0 0 a , 2000b) a n d overlapping foraging a r e a s (Mowrey a n d Z a s a d a 1984; C a r e y et al. 1999; C a r e y 2000), core nest a r e a s (Cotton a n d P a r k e r 2 0 0 0 b ) , a n d h o m e r a n g e s (Witt 1992).  P r e d a t o r s of northern  squirrels include the spotted owl, great horned owl (Bubo barred owl (S. varia Turton), coyote (Canis  Barton), w e a s e l (Mustela  virginianus  (Gmelin)),  spp.), marten (Maries  americana  latrans S a y ) , red fox (Vulpes  rufus S c h r e b e r ) , a n d lynx (Lynx canadensis  flying  vulpes  L i n n a e u s ) , b o b c a t (Lynx  Kerr) (reviewed  in W e l l s G o s l i n g a n d  H e a n e y 1984). Truffles (described  below) are a predominant food of northern flying squirrels  in the P a c i f i c Northwest (Table 1).  A n a l y s e s of s t o m a c h contents or f e c a l pellets  indicate that northern flying squirrels generally c o n s u m e arboreal lichens during the s n o w - c o v e r e d period ( M c K e e v e r 1960; W e i g l 1978; M a s e r et al. 1985, 1986; Hall 1 9 9 1 ; Rosentreter et al. 1997; but s e e C u r r a h et al. 2000) a n d truffles during the  5 r e m a i n d e r of the y e a r (Table 1). Northern flying squirrels w e r e not o b s e r v e d to dig under the s n o w for fungi (Hall 1991) leading s o m e authors to s p e c u l a t e that truffles (Hall 1991) or m u s h r o o m s (Currah et al. 2000) occurring in the winter diets of northern flying squirrels inhabiting s n o w - c o v e r e d a r e a s m a y be taken from food c a c h e s of other sciurid s p e c i e s .  M o w r e y a n d Z a s a d a (1984) o b s e r v e d northern  flying squirrels raiding c a c h e d fungi from red squirrel (Tamiasciurus E r x l e b e n j m i d d e n s in A l a s k a .  hudsonicus  In a r e a s with mild winters a n d no s n o w c o v e r or  frozen ground conditions, truffles m a y be a c c e s s i b l e a n d available year-round ( M a s e r et al. 1986; M a s e r a n d M a s e r 1988; C o l g a n 1997; North etal.  1997; T h y s e l l  et al. 1997), but are l e s s a b u n d a n t in the winter (Hunt a n d T r a p p e 1987; North et al. 1997). In m a n y studies, arboreal lichens w e r e a b u n d a n t year-round within the study a r e a but w e r e either a b s e n t from or represented a minor c o m p o n e n t of the spring, s u m m e r , a n d fall diets of northern flying squirrels inhabiting t h e s e sites ( M a s e r et al. 1 9 7 8 a , 1 9 8 5 ; Hall 1 9 9 1 ; C a r e y 1995; C o l g a n 1997).  H o w e v e r , lichen w a s a  dominant food item in the spring ( P y a r e a n d L o n g l a n d 2 0 0 1 a ) a n d s u m m e r (Waters a n d Z a b e l 1995) diets of northern flying squirrels in fir forests of California, a n d the spring diet of northern flying squirrels in m i x e d w o o d forests in W e s t Virginia (Mitchell 2001).  Northern flying squirrels c o n s u m e m u s h r o o m s a n d other e p i g e o u s fungi  (Table 1), w h i c h range from incidental ( C o l g a n 1997; C a z a r e s et al. 1999) to dominant (Rosentreter et al. 1997; C u r r a h et al. 2000) s e a s o n a l f o o d s . Northern  flying  squirrels  also  eat  plant  material,  including  vegetative  structures (e.g. leaves), staminate c o n e s a n d pollen, roots, b u d s , flowers, fruits, mast, s e e d s , a n d s a p ( W e l l s - G o s l i n g a n d H e a n e y 1984; T a b l e 1). A l t h o u g h plant material often w a s a minor c o m p o n e n t of their overall diet ( C o l g a n 1997; C a r e y et al.  6 1999; C u r r a h et al. 2000), plant material w a s a dominant item in the fall diets of northern flying squirrels in O r e g o n ( C a z a r e s et al. 1999) a n d in W e s t Virginia (Mitchell 2001) a n d in the diet of northern flying squirrels during snow-free periods in A l a s k a ( P y a r e et al. 2002).  C a u t i o n m u s t b e u s e d w h e n determining f o o d items  c o n s u m e d by northern flying squirrels through e x a m i n a t i o n of f e c a l material, s i n c e highly digestible plant parts c a n be u n d e r - r e p r e s e n t e d in s u c h a n a l y s e s (Neal et al. 1 9 7 3 ; Mclntire a n d C a r e y 1 9 8 9 ; T h y s e l l et al. 1997).  What are h y p o g e o u s f u n g i ? H y p o g e o u s fungi are a group of both related a n d unrelated taxa that d e v e l o p h y p o g e o u s (subterranean) fruitbodies, c o m m o n l y referred to a s truffles. Truffles are reproductive  structures  (sporocarps)  that  typically  contain  sexual  propagules  (spores) in fertile t i s s u e s (gleba) e n c l o s e d by a n outer layer or peridium ( J o h n s o n 1996).  T h e A s c o m y c o t i n a , B a s i d i o m y c o t i n a , a n d Z y g o m y c o t i n a s u b d i v i s i o n s all  include h y p o g e o u s s p e c i e s ( C a s t e l l a n o e r a / . 1989). H y p o g e o u s fungi are heterotrophic, a n d a s s u c h , must obtain organic c a r b o n s o u r c e s from other o r g a n i s m s .  H y p o g e o u s fungi d o this by forming a mycorrhizal  a s s o c i a t i o n with roots of v a s c u l a r plants, w h e r e b y both partners enter into a mutualistic  s y m b i o s i s (Fogel  1976;  M a s e r et  al.  1978b,  1985,  1986).  mycorrhizal s y m b i o s i s h a s not b e e n confirmed for all h y p o g e o u s s p e c i e s . this c o n n e c t i o n , the fungi  translocate water,  minerals a n d  nutrients  This  Through from  the  substrate to the host plant a n d obtain photosynthates from t h e s e hosts ( M a s e r et al. 1978b, 1985, 1986; T r a p p e a n d M a s e r 1977; A l l e n 1 9 9 1 ; Smith a n d R e a d 1997). In addition to extending the host root s y s t e m ( F o g e l 1976), mycorrhizal fungi a l s o c a n protect host roots from p a t h o g e n s a n d bacteria (Trappe a n d M a s e r 1977; M a s e r et  T a b l e 1.  S u m m a r y of studies d e s c r i b i n g the diet of northern flying squirrels in the wild. V a l u e s are s u m m a r i z e d or reported directly from tables, e s t i m a t e d from graphs, or obtained from information in the text.  Principal Foods of Northern Flying Squirrels by Season 3  Summer  Fall  Ecosystem  Spring  P i n e a n d fir forests in C a l i f o r n i a  Apr. - Jun.: lichens (90%), fungi (10%)  C o n i f e r o u s forests in O r e g o n  Not divided by season: truffles (78% by v o l u m e of S C , 9 2 % of s a m p l e s )  Jul. - Sept.: fungi (100%)  Oct. - Dec: fungi (53 70%), lichens (30 - 4 7 % )  Mature (150-yearold) white s p r u c e forests in A l a s k a  m u s h r o o m s & truffles (fresh a n d dried), berries, lichens  Old-growth Douglas-fir forests in northwest Oregon  truffles a n d unidentified fungi (100%)  Winter Jan. - Mar.: lichens (90 100%), fungi (10%), meat (5%)  c a c h e d fungi, lichens  Source of diet analysis 6  " S C (N=24)  M c K e e v e r (1960)  **SC & FP (N=12)  M a s e r et al. (1978a)  D O (N=12 squirrels)  Mowrey and Z a s a d a (1984)  *SC & FP (N=21)  M a s e r etal: (1985)  Old-growth l o d g e p o l e pine a n d mixed conifer forests in northeast Oregon  May & June: lichens (61 6 8 % ) , conifer flowers (14% • May)  Jul.: truffles (50%), unidentified fungi (18%), l i c h e n s (22%), mushrooms  Sept. - Oct.: truffles (56%), mushrooms (35%), lichens (8%)  Dec. - April: lichens (93%)  *SC & FP (N=61)  Old-growth Douglas-fir forests in southwestern Oregon  Apr. - June: truffles (100%), mushrooms (25%)  Jul. - Sept.: truffles (90 100%), mushrooms (23%)  Oct. - Dec: truffles (100%), mushrooms (23%)  Jan. - Mar.: lichens (34%)  * F P (N=162) (monthly samples)  7  Reference  M a s e r et al. (1986)  T a b l e 1.  (continued)  Principal Foods of Northern Flying Squirrels by Season 3  Ecosystem  Spring  Summer  Fall  Old-growth Douglas-fir forests in O r e g o n  truffles (100%)  High elevation, mixed conifer forests in California  Snow-free period: (1 Jun. - 15 Nov.): 10 truffle g e n e r a (12 - 9 2 % ) , 2 puffball g e n e r a (8% & 2 2 % ) , 3 lichen g r o u p s (8 - 1 3 % ) , 1 m u s h r o o m g e n u s (13%)  Y o u n g (44- to 6 7 year-old) a n d o l d growth ^ 2 5 0 - y e a r old) Douglas-fir forests in southwest O r e g o n Y o u n g (44- to 6 7 year-old) a n d o l d growth (> 2 5 0 year-old) w e s t e r n hemlock forests in western Washington O l d (> 2 0 0 - y e a r old) fir forests in northeast California  Not divided by seasons (collected in spring and fall): Y o u n g : 8 truffle g e n e r a (10 - 1 0 0 % ) , m u s h r o o m s (75%)  Winter  Snow-covered period: (16 Nov. - 31 May): 9 truffle g e n e r a (6 - 81%), 3 lichen groups (34 - 4 5 % ) , 1 m u s h r o o m g e n u s (32%), 1 puffball g e n u s (11%)  Source of diet analysis**  Reference  * F P (N=10)  Mclntire a n d C a r e y (1989)  * F P (N=93), S C (N=14)  Hall (1991)  ^ F P (mean values)  C a r e y 1995  * F P (N=88) (over two years)  Waters and Zabel (1995)  Not divided by seasons (collected in spring and fall): Old-growth: 10 truffle g e n e r a (5 - 88%), m u s h r o o m s (63%), plant material (12%) Not divided by seasons (collected in spring and fall): Y o u n g : 6 truffle g e n e r a (6 - 1 0 0 % ) , m u s h r o o m s (18%), plant material (11 %) Not divided by seasons (collected in spring and fall): Old-growth: 7 truffle g e n e r a (10 - 1 0 0 % ) , m u s h r o o m s (36%), plant material (9%) Jul. - Sept.: truffles (100%), lichens ( 7 0 % ) , plant material (66%), insects (20%), m u s h r o o m s (19%), conifer staminate c o n e s (15%)  8  T a b l e 1.  (continued)  Principal Foods of Northern Flying Squirrels by Season 3  Ecosystem  Spring  Summer  Fall  Winter  Jan.: 6 truffle g e n e r a (7 - 8 3 % ) , plant material (19%)  5 5 - to 65-year-old Douglas-fir forests in W a s h i n g t o n  3  * F P (N=67)  Jul. - Sept.: truffles (100%), plant material (64%), lichens (60%), m u s h r o o m s (28%), conifer staminate c o n e s (25%), insects (13%)  Y o u n g (75- to 9 5 year-old) fir forests in northeast California  Source of diet analysis*  T  F P (N=11)  Reference Waters and Zabel (1995) continued.  C o l g a n et al. (1997)  4 truffle g e n e r a (7 2 7 % ) , plant material (7%)  5 truffle g e n e r a (6 - 2 0 % ) , plant material (7%)  T C  FP(N=185) (pooling method)  C o l g a n (1997), C a r e y et al. (2002)  High elevation conifer forests in central Idaho  Snow-free period (Jun. - Aug.): m u s h r o o m s (7 - 7 8 % ) , 4 truffle g e n e r a (8 - 3 8 % ) , l i c h e n s (25%), plant material (25%)  Snow-covered period: lichens (86%), m u s h r o o m s (63 77%), 4 truffle g e n e r a (8 - 7 6 % )  * F P (N=200) (from nest boxes)  Rosentreter et al. (1997)  5 0 - to 70-year-old Douglas-fir a n d m i x e d w o o d forests in W a s h i n g t o n  Apr. - June: truffles (84%), e p i g e o u s fungi (11%), plant material (5%)  * D O (N=63 observations, N=43 squirrels)  T h y s e l l et al. (1997)  Jul. - Sept.: truffles (64%), e p i g e o u s fungi (27%), plant material (9%)  Oct. - Dec: e p i g e o u s fungi (64%), truffles (18%), plant material (18%)  9  Jan. - Mar.: e p i g e o u s fungi (55%), plant material (27%), truffles (18%)  T a b l e 1.  (continued)  Principal Foods of Northern Flying Squirrels by Season 3  Ecosystem  Spring  Summer  Fall  Winter  7 to 9 truffle g e n e r a (8 100%), plant material  (too few samples)  1 1 0 - t o 130-yearold Douglas-fir forests in O r e g o n  4 truffle g e n e r a (10 9 9 % ) , plant material (7 29%)  4 truffle g e n e r a (21 - 1 0 0 % ) , plant material (52%)  High elevation coniferous / northern h a r d w o o d forests in north Carolina & Tennessee  Not divided by season: 4 truffle g e n e r a (~5 - 9 5 % ) , m u s h r o o m s ( - 2 0 % ) , plant material c o n s u m e d 'in a m o u n t s suggesting substantial and frequent ingestion'.  Old-growth (> 2 5 0 year-old) red fir forests in California  Late May - early Jul.: truffles (100%), m u s h r o o m s ( - 4 5 % ) , plant material ( - 4 0 % ) , lichens ( - 3 5 % )  Aug. - early Oct.: truffles (100%), m u s h r o o m s ( - 3 0 % ) , plant material ( - 3 7 % ) , lichens (-5%)  10  Reference (1999)  FP (N = 24)  C a z a r e s et al. (1999)  *FP(N=116) (analyzed for fungal spores only - plant material not quantified)  W e i g l et al. (1999)  * G C (N=138) * F P (N=110) presented, s e e reference  C u r r a h et al. (2000)  * F P (N=93)  Pyare and L o n g l a n d (2001a)  T  3 mushrooms groups ( 6 5 % 9 1 % ) , 3 truffle g e n e r a (7 19%)  3 mushroom g r o u p s (15 4 5 % ) , 4 truffle g e n e r a (9 18%), other fungi ( 6 - 1 3 % )  3  C a r e y etal.  T h r e e (40- to 3 5 0 year-old) forest types in southwestern  M i x e d w o o d boreal forest in northeastern Alberta  Source of diet analysis*  T a b l e 1.  (continued)  Principal Foods of Northern Flying Squirrels by Season Winter Summer Fall Spring 3  Ecosystem Mature s p r u c e / northern h a r d w o o d forests in w e s t Virginia  Old-growth conifer forests a n d mixed conifer-muskeg habitats in southeast A l a s k a  lichens (83%), plant buds (10 - 63%), 1 truffle g e n u s (51 %), insects (22%), plant material (14%)  1 truffle g e n u s (48%), nut/fruit (43%), plant material (34%), insects (25%), lichens (23%), mushrooms (20 - 23%), plant buds & m o s s e s (11%) During the snow-free period: Old-growth: 5 5 % plant material, 5 0 % truffles, 3 6 % m u s h r o o m s , 2 7 % lichens  —  Source of diet analysis^ * F P (ISM 15)  T  F P (N=168)  Reference Mitchell (2001)  P y a r e er al. (2002)  During the snow-free period: Muskeg stands: 5 9 % m u s h r o o m s , 4 6 % vegetation, 2 0 % l i c h e n s , 1 9 % truffles  Principal foods are: 1) p r e s e n t o n m i c r o s c o p e slides with a m e a n percent o c c u r r e n c e of at least 5 % of the fields of view ( C o l g a n 1997) for all s a m p l e s collected within e a c h s e a s o n (termed 'relative a b u n d a n c e ' in C u r r a h et al. 2000); or 2) present in at least 5 % of the s a m p l e s collected within e a c h s e a s o n (termed 'frequency' in Currah et al. 2000); or 3) p r e s e n t in at least 5 % by v o l u m e of s t o m a c h contents ( S C ) ; or 4) c o m m o n l y c o n s u m e d by feeding squirrels during direct behavioural observations. Source of diet analysis includes F P (fecal pellets), G C (gut contents), S C (stomach contents), and/or D O (direct observation). N = n u m b e r of s a m p l e s ( F P , S C ) or n u m b e r of individual squirrels ( D O ) or individual observations (DO), if given. T h e m e t h o d of describing the diet within e a c h s e a s o n is a s follows (values are presented in parentheses):  a  b  11  T h e m e a n relative a b u n d a n c e of e a c h item in the diet T h e percent f r e q u e n c y of s a m p l e s containing a principal food item T h e m e a n p e r c e n t a g e by v o l u m e of s t o m a c h contents of e a c h food item T h e f r e q u e n c y of o b s e r v a t i o n s of individuals c o n s u m i n g a food item R e l a t i v e f r e q u e n c y is calculated by s u m m i n g the m e a n percent frequency of o c c u r r e n c e for all food items, a n d dividing e a c h by the total ( C o l g a n 1997; C a r e y et al. 1999). +  c  12  13 al. 1978b; L a u r s e n 1985). T h e mycorrhizal a s s o c i a t i o n often is e s s e n t i a l for growth, persistence, a n d ultimately survival of both fungus a n d host Smith a n d R e a d 1997).  ( M a s e r et al. 1978b;  Mycorrhizal fungi are a s s o c i a t e d with the roots of most  v a s c u l a r plants {reviewed in A m a r a n t h u s 1998), including m e m b e r s of the P i n a c e a e , F a g a c e a e , E r i c a c e a e , S a l i c a c e a e , a n d B e t u l a c e a e families, although the d e g r e e of host specificity varies a m o n g mycorrhizal fungal s p e c i e s studied to date (Trappe a n d M a s e r 1977; M o l i n a etal. 1992; Horton a n d B r u n s 1998). Mycorrhizal fungi play important roles in forested e c o s y s t e m s , functioning in forest productivity ( F o g e l a n d Hunt 1979; V o g t et al. 1981), nutrient cycling, a n d energy flow (Harley 1 9 7 1 ; F o g e l a n d T r a p p e 1978; F o g e l a n d Hunt 1979; F o g e l 1980,  1981; Vogt and  E d m o n d s 1980; A m a r a n t h u s  and  P e r r y 1994).  Their  fruitbodies are a l s o a n important food s o u r c e for m a n y a n i m a l s (Fogel 1976; F o g e l a n d T r a p p e 1978; M a s e r et al. 1978a).  Mycophagy in forested ecosystems M y c o p h a g y , or the c o n s u m p t i o n of fungi by a n i m a l s , is c o m m o n in forested e c o s y s t e m s (Fogel a n d T r a p p e 1978; M a s e r et al. 1978a). T h e importance of fungi in the diet of a n i m a l s c a n range from incidental feeding to d e p e n d e n c e on fungi a s a dominant food item (e.g. California r e d - b a c k e d vole (Clethrionomys  californicus  Merriam), M a s e r et al. 1 9 7 8 a ; U r e a n d M a s e r 1 9 8 2 ; northern flying squirrel, T a b l e 1) a n d c a n vary with s e a s o n ( H a y e s et al. 1986; B o z i n o v i c a n d M u n o z - P e d r e r o s 1995), habitat ( M a s e r et al. 1978a), a n d fungal availability (Claridge et al. 1 9 9 3 a ; J o h n s o n 1994b, 1994c).  Truffles are c o n s u m e d by a wide variety of a n i m a l s (reviewed  in  F o g e l a n d T r a p p e 1978), most notably s m a l l to m i d - s i z e d m a m m a l s (e.g. M a s e r et al. 1 9 7 8 a , 1 9 8 5 , G r o n w a l l a n d P e h r s o n 1984; B l a s c h k e a n d B a u m l e r 1989; C a z a r e s  14 a n d T r a p p e 1994; C l a r i d g e a n d C o r k 1994; J o h n s o n 1 9 9 4 a , 1 9 9 4 c ; B o z i n o v i c a n d M u f i o z - P e d r e r o s 1995) but a l s o by s o m e invertebrates (e.g. M c l l v e e n a a n d C o l e 1976; North e r a / . 1997) a n d large m a m m a l s (e.g. T r a p p e a n d M a s e r 1977; C a z a r e s a n d T r a p p e 1994). S p o r e s from e p i g e o u s (above-ground) m u s h r o o m s c a n effectively d i s p e r s e via non-biotic vectors s u c h a s wind a n d water.  S i n c e truffles fruit Underground,  a n i m a l m y c o p h a g i s t s are the primary d i s p e r s a l a g e n t s for h y p o g e o u s taxa (Trappe a n d M a s e r 1977; M a s e r et al. 1 9 7 8 a , 1979b).  M a m m a l m y c o p h a g i s t s detect a n d  distinguish s p e c i e s of truffles by their characteristic o d o u r ( C l a u s et al. 1 9 8 1 ; M a s e r et al. 1985; Z a b e l a n d W a t e r s 1997), w h i c h intensifies a s s p o r o c a r p s mature ( F o g e l a n d T r a p p e 1 9 7 8 ; M a s e r et al. 1978b).  Following e x c a v a t i o n , truffles with s p o r e s  e m b e d d e d throughout the fleshy fruitbodies are c o n s u m e d by a n i m a l s a n d are d e p o s i t e d throughout the forest in their f e c e s ( M a s e r et al. 1978b; C o r k a n d K e n a g y 1989a).  F o r t h o s e truffles containing a n inner powdery s p o r e m a s s s u r r o u n d e d by  a n outer shell (peridium) at maturity (e.g. m e m b e r s of Elaphomyces),  some spores  are ingested with the peridium (Cork a n d K e n a g y 1 9 8 9 a , 1989b) a n d the rest are d i s c a r d e d or d r o p p e d during c o n s u m p t i o n a n d d i s p e r s e d via wind (Trappe  and  M a s e r 1977; C o r k a n d K e n a g y 1989b; Z a b e l a n d W a t e r s 1997). S p o r e s remain undigested (Cork a n d K e n a g y 1 9 8 9 a , 1989b) a n d viable (Trappe a n d M a s e r 1976; Kotter a n d Farentinos 1984; C l a r i d g e et al. 1992; C o l g a n a n d C l a r i d g e 2002) after p a s s a g e through the digestive tracts of a n i m a l s . A l o n g with concentrations of fungal s p o r e s , f e c a l pellets contain y e a s t s , nitrogen-fixing bacteria, a n d nutrients (Li et al. 1986), w h i c h m a y facilitate s p o r e germination (Li et al. 1986; M a s e r a n d M a s e r 1988).  G e r m i n a t i o n of fungal s p o r e s m a y b e e n h a n c e d (Lamont  et al. 1985; C o r k a n d K e n a g y 1989b; C l a r i d g e et al. 1992; C o l g a n a n d C l a r i d g e  15 2002) or unaffected (Kotter a n d Farentinos 1984; C o l g a n a n d C l a r i d g e 2002) by animal consumption. T h e role of particular s p e c i e s of m y c o p h a g i s t s a s d i s p e r s a l vectors for h y p o g e o u s s p o r e s d e p e n d s on the proportion of fungi in their diet a n d the b e h a v i o u r of the a n i m a l ( M a s e r et al. 1 9 7 8 a , 1978b). S p e c i e s s u c h a s d e e r mice maniculatus  W a g n e r ) a n d c h i p m u n k s (Tamias  {Peromyscus  spp.) that frequent e d g e or newly  disturbed habitats m a y play a n important role in colonizing early s u c c e s s i o n a l or non-forested sites ( M a s e r et al. 1 9 7 8 a , 1978b; Li et al. 1986; C a z a r e s a n d T r a p p e 1994).  S p e c i e s s u c h a s northern flying squirrels that generally remain in forested  habitats m a y provide further inoculation of n e w host plant roots ( M a s e r et al. 1 9 7 8 a , 1978b, Li er al.  1986) a n d help maintain the g e n e t i c diversity of  mycorrhizal  c o m m u n i t i e s (Claridge et al. 1992; C o l g a n a n d C l a r i d g e 2002). D u e to their s u b t e r r a n e a n fruiting habit, truffles are protected from d e s i c c a t i o n a n d e x t r e m e s in temperature (Wilkins a n d Harris 1946; J o h n s o n 1996) a n d m a y therefore be a m o r e stable food for m y c o p h a g o u s a n i m a l s than a b o v e - g r o u n d fungi s u c h a s m u s h r o o m s (Blair et al. 1984; North et al. 1997).  T h e prolific fruiting  characteristic of s o m e truffle s p e c i e s c a n result in a b u n d a n t food r e s o u r c e s in s o m e habitats (Cork a n d K e n a g y 1989b; L u o m a 1991). H o w e v e r , m y c o p h a g y r e d u c e s the n u m b e r of truffles in a n a r e a , a n d s i n c e m a n y s m a l l m a m m a l s rely on truffles a s their primary food (Fogel a n d T r a p p e 1978) this reduction c a n be significant. example,  in  western  hemlock  (Tsuga  heterophylla  (Raf).  Sarg.)  forests  For in  W a s h i n g t o n , North et al. (1997) c o m p a r e d the b i o m a s s of truffle s p e c i e s found in o p e n plots to t h o s e found in plots under e x c l o s u r e s a n d reported significantly higher standing crop of truffles under e x c l o s u r e plots. T h e a v e r a g e c o n s u m p t i o n of truffles e x c e e d e d their production in y o u n g , m a n a g e d s t a n d s in winter in the a r e a s studied  16 (North et al. 1997). U s i n g a similar o p e n v e r s u s e x c l o s u r e plot c o m p a r i s o n , J o h n s o n (1994b) reported 'substantial' harvesting rates (up to 7 0 % of s p o r o c a r p s of s o m e truffle s p e c i e s ) by a rat k a n g a r o o ( T a s m a n i a n bettong Bettongia  gaimardi  (Desm.))  in eucalypt forests of T a s m a n i a . S i n c e certain truffle s p e c i e s are preferentially e a t e n (Ure a n d M a s e r 1982; J o h n s o n 1994b; North et al. 1997), their production c a n be underestimated in field collections ( J o h n s o n 1994b).  The value of truffles as food T h e c o n s u m p t i o n of truffles by m a n y a n i m a l s (reviewed  in F o g e l a n d T r a p p e  1978) c o u p l e d with their significant g r o s s energy content a n d concentrations  of  crude protein, macronutrients a n d minerals, h a v e led m a n y authors to c o n c l u d e that truffles represent a high quality food (Tevis 1952; M c K e e v e r 1960; F o g e l a n d T r a p p e 1978; Blair et al. 1984; G r o n w a l l a n d P e h r s o n 1984; W e i g l et al. 1999).  However,  g r o s s m e a s u r e m e n t s of energy or nutrient content m a y overestimate the a m o u n t of digestible energy or nutrients available to a particular c o n s u m e r . high proportion (Elaphomyces Mesophellia  (>50%) of the total nitrogen  granulatus glauca,  For example, a  present in s e v e r a l truffle s p e c i e s  Fr., C o r k a n d K e n a g y 1989b; Rhizopogon  luteolus  Fr. a n d  C l a r i d g e a n d C o r k 1994; eight s p e c i e s , C l a r i d g e et al. 1999) is  a s s o c i a t e d with indigestible cell walls a n d s p o r e s or o c c u r s in non-protein  forms  (Cork a n d K e n a g y 1989b; C l a r i d g e a n d C o r k 1994; C l a r i d g e et al. 1999) s u g g e s t i n g poor to moderate nutritional C l a r i d g e etal.  quality ( A l e x a n d e r 1994; C l a r i d g e a n d C o r k 1994;  1999).  Truffle s p e c i e s differ in the concentration of food c o m p o n e n t s (Gronwall a n d P e h r s o n 1984; C l a r i d g e a n d C o r k 1994) a n d in the relative digestibility of t h e s e c o m p o n e n t s (e.g. proportion that is present in cell contents rather than b o u n d in cell  17 walls) (Claridge et al. 1999).  T h i s m a y partly explain w h y northern flying squirrels  a p p e a r to prefer certain truffle s p e c i e s to others during cafeteria-style f e e d i n g trials (Zabel a n d W a t e r s 1997) a n d under natural conditions ( C o l g a n 1997; C a r e y et al. 2002).  S t o r a g e a n d s u b s e q u e n t drying of both e p i g e o u s a n d h y p o g e o u s fungi by  tree squirrels during the winter h a s b e e n d o c u m e n t e d (Hardy 1949; S m i t h 1968; Hall 1991); this c o n c e n t r a t e s nutrients by reducing the water content of fruitbodies ( F o g e l 1976; G r b n w a l l a n d P e h r s o n 1984).  T h e a c c u m u l a t i o n of s o m e nutrients within  fruitbodies of truffle taxa varied b e t w e e n s e a s o n s (Blair et al. 1984) a n d different s t a n d s a g e s a n d e c o s y s t e m types (Vogt a n d E d m o n d s 1980). In addition, the a g e of the s p o r o c a r p , the nutrient a n d moisture content of the substrate, a n d the type of substrate (e.g. w o o d y or forest floor) affects the nutrient content of truffles ( F o g e l 1976, V o g t a n d E d m o n d s 1980). G u t m o r p h o l o g y a n d body s i z e of c o n s u m e r s affects the digestive capabilities of a n i m a l s a n d c o n s e q u e n t l y the value of truffles to the c o n s u m e r (Cork a n d K e n a g y 1989b).  M o r p h o l o g i c a l a n d physiological adaptations of the alimentary c a n a l , s u c h  a s the p r e s e n c e of a n enlarged f o r e s t o m a c h or c a e c u m , i n c r e a s e food  retention  v o l u m e a n d time, microbial fermentation, a n d the ability to digest fibre  (Bjornhag  1994;  Hume  1994).  C o l o n i c separation  mechanisms can also increase  the  digestibility of food c o m p o n e n t s (e.g. fibre a n d nitrogen) by permitting retention of bacteria in the proximal colon a n d c a e c u m (Cork a n d K e n a g y 1989b; C l a r i d g e et al. 1999).  S u c h adaptations allow m y c o p h a g i s t s s u c h a s rat-kangaroos (bettongs a n d  potoroos) (with a large f o r e s t o m a c h ; C l a r i d g e a n d C o r k 1994) a n d the California redbacked  vole  (with a  large  caecum  and  a well-developed  colonic  separation  m e c h a n i s m ; C l a r i d g e et al. 1999) to digest f o o d s s u c h a s truffles with greater efficiency.  H o w e v e r , northern flying squirrels, like other sciurids, p o s s e s s a less  18 s p e c i a l i z e d digestive tract (Cork a n d K e n a g y 1989b; C l a r i d g e et al. 1999), w h i c h is reflected in their relatively poor digestion of s o m e s p e c i e s of truffles during feeding trials (Table 2, e . g . C l a r i d g e etal.  1999).  It is unknown if northern flying squirrels practice c o p r a p h a g y or c e c o t r o p h y to re-ingest the m i c r o b e s a n d e n e r g y lost in their f e c e s a n d e n h a n c e digestibility; they h a v e not b e e n o b s e r v e d to d o s o under experimental conditions (Claridge et al. 1999).  In addition, s i n c e the digestibility of truffles h a s b e e n studied using only o n e  s p e c i e s at a time during feeding trials, a n y a s s o c i a t i v e effects in digestibility with mixed truffle diets h a v e not b e e n e x a m i n e d ( B o z i n o v i c a n d M u h o z - P e d r e r o s 1 9 9 5 ; C l a r i d g e etal. 1999). G i v e n the low digestibility of most truffle s p e c i e s studied to date, w h y a r e truffles a primary c o m p o n e n t of the s e a s o n a l or year-round diet of s o m e a n i m a l s s u c h a s the northern flying squirrel? T h e v a l u e of truffles to a n i m a l s m a y b e d u e to their high detectibility a n d low s e a r c h i n g c o s t (Cork a n d K e n a g y 1989b), their minimal handling a n d p r o c e s s i n g time (Smith 1 9 6 8 ; C o r k a n d K e n a g y 1989b), a n d their high s e a s o n a l a b u n d a n c e (Cork a n d K e n a g y 1989b; B o z i n o v i c a n d M u n o z P e d r e r o s 1995). T h e s e factors e n a b l e relatively large g a i n s in e n e r g y relative to the c o s t s of foraging c o m p a r e d to other food items, which m a y h a v e a higher caloric or nutrient content, but a r e l e s s abundant, l e s s detectible, or more o n e r o u s to c o n s u m e (Cork a n d K e n a g y 1989b; B o z i n o v i c a n d M u n o z - P e d r e r o s 1995).  For example,  northern flying squirrels w e r e u n a b l e to maintain their body weight o n a diet of conifer c o n e s during feeding trials (Brink a n d D e a n 1 9 6 6 ; L a u r e n c e a n d R e y n o l d s 1984), e v e n though s e e d s a r e high in digestible protein, energy, a n d lipids (Batzli a n d C o l e 1 9 7 9 ; Martin 1979).  Extracting s e e d s from conifer c o n e s m a y require  greater e n e r g y expenditure for s o m e c o n s u m e r s than the e n e r g y derived from the  T a b l e 2.  T h e apparent digestibility  3  of fungi c o n s u m e d by m y c o p h a g i s t s during feeding trials a n d their digestive  strategies.  California redbacked vole 1  Mean apparent diqestibility (%) Cascade Northern mantled ground flying Longhaired squirrel squirrel field mouse 1  2  3  Long-nosed A Potoroo  RHVI  BOED  RHVI  ELGR  MEGL  RHLU  Dry matter  67.1  48.2  65.9  59.9  86.4  80.1  Total nitrogen  34.8  61.3  11.4  29.9  57.9  46.0  C e l l wall constituents  71.6  —  66.7  53.4  91.9  53.7  Energy  65.4  46.1  61.7  52.2  89.1  75.6  Food item  b  Food component  Digestive strategies of each mycophagist 50.9-55.9  26  B o d y m a s s (g)  147  214-266  852 - 970  EF SS, EC SS, EC SS, EC, C S M Gut morphology a p p a r e n t digestibility = m e a s u r e of ingested f o o d c o m p o n e n t from feeding trial - m e a s u r e of excreted food c o m p o n e n t in 0  a  the f e c a l s a m p l e (Cork a n d K e n a g y 1989b). b  C  R H V I = Rhizopogon  vinicolor;  R H L U = Rhizopogon  luteolus  B O E D = Boletus  edulis;  E L G R = Elaphomyces  granulatus;  M E G L = Mesophellia  glauca;  S S = s i m p l e s t o m a c h (hindgut fermenter); E F = enlarged forestomach (foregut fermenter); E C = enlarged c a e c u m ; C S M = c o l o n i c separation m e c h a n i s m  1  C l a r i d g e et al. (1999); Abrothrix longipilis, a n d K e n a g y (1989b); Potorous tridactylus, 2  4  B o z i n o v i c a n d M u n o z - P e d r e r o s 1 9 9 5 ; Spermophilus C l a r i d g e a n d C o r k (1994) 19 z  saturatus  (Rhoads), Cork  20 food itself ( L a u r e n c e a n d R e y n o l d s 1984). Truffles a l s o m a y provide specific minerals a n d vitamins that m a y be in short supply ( B o z i n o v i c a n d M u h o z - P e d r e r o s 1995) s u c h a s s o d i u m (e.g. granulatus,  Elaphomyces  V o g t a n d E d m o n d s 1 9 8 1 ; G r b n w a l l a n d P e h r s o n 1984) a n d m a y be a n  important s o u r c e of water (Fogel a n d T r a p p e 1978; M a s e r et al. 1978b). T h e e g g s , larvae or adult insects that m a y be present on or in truffles could impart a n a d d e d nutritional benefit  to m y c o p h a g i s t s ( B o z i n o v i c a n d  M u h o z - P e d r e r o s 1995).  A  b a l a n c e d or a d e q u a t e diet m a y be attained through o c c a s i o n a l c o n s u m p t i o n of other higher quality food items (Smith 1968; C o r k a n d K e n a g y 1989b; B o z i n o v i c a n d M u h o z - P e d r e r o s 1995) in addition to fungi. A n i m a l s likely d o not u s e energetic or nutritional criteria a l o n e in the selection of food items.  Palatability ( F o g e l a n d T r a p p e 1978), limitations of m e m o r y (Belisle  a n d C r e s s w e l l 1997), the p r o c e s s of learning a n d influence of a g e (Galef 1 9 9 3 ; G o s s e l i n a n d C h i a 1996), a n d eating f o o d s that are most familiar (Partridge 1981) m a y lead to foraging behaviour that d o e s not result in the selection of the most energetic or nutritional food types.  Exploratory behaviour, rather than energy gain  ( F o r k m a n 1996) could at times drive foraging behaviour.  For whatever reason,  northern flying squirrels consistently preferred s o m e truffle s p e c i e s to lichens a n d fir s e e d s during experimental feeding trials (Zabel a n d W a t e r s 1997).  Determining mycophagist diets Microhistological a n a l y s i s of s t o m a c h contents or f e c a l pellets c a n be u s e d to determine the h y p o g e o u s taxa c o n s u m e d by a m y c o p h a g i s t ( C a s t e l l a n o et al. 1989; Mclntire a n d C a r e y 1989).  S t o m a c h contents m a y provide a more c o m p l e t e (i.e.  undigested) representation of a n a n i m a l ' s last m e a l (Ure a n d M a s e r 1982); however,  21 this  method  n e c e s s i t a t e s sacrificing individuals, w h i c h  e c o l o g i c a l studies undigested  (Mclntire  remains  of  an  and  C a r e y 1989).  individual's  is undesirable in  many  F e c a l s a m p l e s represent  previous  meal(s),  and  the  microscopic  examination of f e c a l material is a c o m m o n l y u s e d a p p r o a c h to determine o c c u r r e n c e of fungal s p o r e s in a n a n i m a l ' s diet (Mclntire a n d C a r e y 1989).  the The  fungal c o m p o n e n t of the diet m a y be more broadly represented in f e c a l material than s t o m a c h contents, s i n c e pellet collections often contain the r e m a i n s of m o r e than o n e m e a l (Mclntire a n d C a r e y 1989). T h e rate of p a s s a g e of fungal s p o r e s through the gut d e p e n d s o n the a m o u n t of food a n d s p e c i e s of fungi c o n s u m e d a n d the gut morphology, body s i z e , a n d activity  levels of the  a n i m a l c o n s u m e r (Bozinovic a n d  M u n o z - P e d r e r o s 1995;  C l a r i d g e et al. 1999). M o s t (95%) of the fungal s p o r e s c o n s u m e d by golden-mantled ground squirrels {Spermophilus  lateralis  S a y , C o r k a n d K e n a g y 1989a) a n d long-  n o s e d potoroos (Claridge a n d C o r k 1984) during feeding trials w e r e excreted within a 4 8 - h o u r or 2 5 - to 30-hour period, respectively. C l a r i d g e et al. (1999) estimated a m e a n retention time of 15.5 hours for digestia to p a s s through the gastrointestinal tracts of northern flying squirrels. Direct o b s e r v a t i o n s of a n i m a l ' s feeding  b e h a v i o u r c a n a l s o be u s e d to  d o c u m e n t dietary items (Mowrey a n d Z a s a d a 1984; T h y s e l l et al. 1997), a n d is e s p e c i a l l y effective for recording highly digestible f o o d s that m a y be indiscernible in s t o m a c h or f e c a l contents (Mclntire a n d C a r e y 1989).  H o w e v e r , this a p p r o a c h c a n  be challenging with a nocturnal, arboreal, a n d highly mobile s p e c i e s s u c h a s the northern flying squirrel (Thysell et al. 1997).  22  Patterns of truffle occurrence, distribution, and abundance Truffles represent a temporally and spatially variable food s o u r c e for a n i m a l s . T h e o c c u r r e n c e a n d a b u n d a n c e of truffle s p e c i e s c h a n g e through time, s h o w i n g s e a s o n a l a n d a n n u a l variation (Fogel 1976; Hunt a n d T r a p p e 1987; L u o m a et al. 1 9 9 1 ; C l a r i d g e et al. 1993b, 2 0 0 0 a ; J o h n s o n 1 9 9 4 a ; S t a t e s a n d G a u d 1997) in r e s p o n s e to climatic conditions s u c h a s rainfall and temperature (Wilkins a n d Harris 1946; F o g e l 1976; Hunt a n d T r a p p e 1987; L u o m a et al. 1 9 9 1 ; J o h n s o n 1 9 9 4 a ; S t a t e s a n d G a u d 1997).  Truffle production in a stand fluctuates from y e a r to year,  month to month (Fogel 1976; Hunt a n d T r a p p e 1987; L u o m a e r a / . 1 9 9 1 ; C l a r i d g e et al. 1993b; J o h n s o n 1 9 9 4 a ; S t a t e s and G a u d 1997) a n d e v e n w e e k to w e e k (Fogel 1976; V o g t et al. 1992).  However, the n u m b e r a n d b i o m a s s of truffles usually are  higher in the spring (Fogel 1976; Hunt a n d T r a p p e 1987; L u o m a et al. 1991) a n d fall (Fogel 1976; F o g e l and Hunt 1979; V o g t et al. 1 9 8 1 ; C l a r i d g e et al. 1993b, 2 0 0 0 a ; S t a t e s a n d G a u d 1997) than s u m m e r (but see L u o m a et al. 1 9 9 1 ; North et al. 1997) and winter (Fogel 1976; F o g e l a n d Hunt 1979; Hunt a n d T r a p p e 1987; North et al. 1997; S t a t e s a n d G a u d 1997). Truffles a l s o s h o w spatial variation with individuals occurring in non-uniform patterns a c r o s s the l a n d s c a p e (Fogel 1976, 1 9 8 1 ; S t a t e s 1 9 8 5 ; Hunt a n d T r a p p e 1987; V o g t et al. 1992). C l u s t e r patterns of truffles are s p e c i e s - s p e c i f i c (Fogel 1976; North and G r e e n b e r g 1998) and range from a scattering of a few individuals to d e n s e aggregations over a n equivalent a r e a (Fogel 1976; Hunt a n d T r a p p e 1987; North and G r e e n b e r g 1998).  C l u s t e r s of truffles typically peak within 2 m of the  nearest live tree (Fogel 1976; S t a t e s 1 9 8 5 ; C l a r i d g e et al. 1993b; J o h n s o n 1 9 9 4 a ; North and G r e e n b e r g 1998) a n d c a n be c l o s e together or widely d i s p e r s e d in a stand (North a n d G r e e n b e r g 1998).  S o m e truffle s p e c i e s a p p e a r to be a s s o c i a t e d  23 with particular substrates s u c h a s c o a r s e w o o d y debris ( A m a r a n t h u s et al. 1994; C l a r k s o n a n d Mills 1994; P y a r e a n d L o n g l a n d 2 0 0 1 b ) , thick organic mats ( J o h n s o n 1994b; North a n d G r e e n b e r g 1998), thin litter layers ( J o h n s o n 1994b; C l a r i d g e etal. 2000b) or with particular s p e c i e s ( F o g e l 1976, 1 9 8 1 ; V o g t et al. 1992; C l a r i d g e et al. 1993b; S t a t e s a n d G a u d 1997; W a t e r s etal.  1997; North a n d G r e e n b e r g 1998) a n d  a g e s (Vogt et al. 1 9 8 1 ; L u o m a et al. 1 9 9 1 ; C a r e y 1995) of host trees.  Since small  m a m m a l s d i s p e r s e fungal s p o r e s via their fecal d e p o s i t s , locations of truffle clusters could a l s o be a s s o c i a t e d with a r e a s of s m a l l m a m m a l u s e s u c h a s latrine sites ( M a s e r et al. 1978b) a n d s m a l l m a m m a l runways along d o w n e d w o o d ( C l a r k s o n a n d Mills 1994).  P y a r e a n d L o n g l a n d (2001b) reported a t e n d e n c y for truffles to fruit in  similar locations a n d times during a three-year study. F u n g a l s u c c e s s i o n (Vogt et al. 1992) a n d competition (Vogt etal. 1992; B r u n s 1995; North etal. 1997) m a y a c c o u n t for a non-overlapping distribution of s p o r o c a r p s a m o n g s o m e truffle s p e c i e s . Local  factors  also  affect  the  resources  and  conditions  necessary  for  d e v e l o p m e n t a n d maturation of truffles (Fogel 1976; Hunt a n d T r a p p e 1987; V o g t et al. 1992; North et al. 1997).  T r e e s p e c i e s a n d density affect the distribution a n d  a m o u n t of fine roots in a n a r e a a n d the availability of host trees for mycorrhizal h y p o g e o u s fungi (Fogel 1976; W a t e r s et al. 1994; Griffiths et al. 1996; North et al. 1997). Nutrient availability in the soil a n d the energy a n d nutrient levels both in host plants a n d the fungal m y c e l i u m m a y affect the o c c u r r e n c e (Hunt a n d T r a p p e 1987; V o g t et. al. 1992; C l a r i d g e et al. 2000b) a n d overall production (Krueger a n d T r a p p e 1967; V o g t  et  al.  1992;  C l a r i d g e et  al.  1993b; J o h n s o n  1994a)  of  truffles.  V e g e t a t i o n , topography, s l o p e (position a n d degree), a s p e c t , a n d g e o l o g y of the site affect microhabitat conditions s u c h a s the a m o u n t of s o l a r radiation a n d rainfall that r e a c h e s the ground, the evaporation levels, d r a i n a g e patterns, a n d the nature a n d  24 type of substrates (Wilkins a n d Harris 1946; F o g e l 1976; V o g t et al. 1992; North et al. 1997; C l a r i d g e et al. 2 0 0 0 b ) .  E d a p h i c conditions, including soil type, moisture,  a n d temperature, are a s s o c i a t e d with the g e n e s i s , maturation, a n d p e r s i s t e n c e of truffles ( F o g e l 1976; Hunt a n d T r a p p e 1987; J o h n s o n 1 9 9 4 a ; C l a r i d g e etal.  2000b)  a n d the distribution a n d relative a b u n d a n c e of truffle s p e c i e s (Claridge et al. 2 0 0 0 b ) . U n f a v o u r a b l e conditions for vegetative  growth (Wilkins a n d Patrick 1940)  and  removal of host trees during harvest ( C o l g a n 1997) a l s o m a y promote the production of fungal fruitbodies.  F o r e x a m p l e , C o l g a n (1997) o b s e r v e d i n c r e a s e d fruiting of  s o m e truffle s p e c i e s in heavily thinned Douglas-fir s t a n d s a n d h y p o t h e s i z e d that this pattern could be d u e to a fungal 'stress reaction', resulting in a greater allocation of energy to the formation of fungal reproductive structures under a d v e r s e conditions a s s o c i a t e d with harvest. E v e n given suitable r e s o u r c e s a n d conditions to e n a b l e fruiting, h y p o g e o u s s p e c i e s s h o w characteristic fruiting strategies ( J o h n s o n 1994a) a n d t e n d e n c i e s to p r o d u c e truffles.  F o r e x a m p l e , W i l k i n s a n d Harris (1946), J o h n s o n (1994a), a n d  S t a t e s a n d G a u d (1997)  all reported  s p e c i e s - s p e c i f i c d e l a y s in truffle fruiting  following favourable climatic conditions.  B e c a u s e of variation a m o n g s p e c i e s in the  t e n d e n c y to fruit, the density of truffles m a y not reflect the b i o m a s s of their m y c e l i a or the levels of inoculation of host roots in a n a r e a (Dahlberg a n d Stenlid 1 9 9 5 ; G a r d e s a n d B r u n s 1996).  H y p o g e o u s s p e c i e s a l s o c a n differ in their periodicity,  longevity, a n d s e a s o n a l i t y of fruiting ( F o g e l 1976; Hunt a n d T r a p p e 1987; L u o m a et al. 1 9 9 1 ; V o g t et al. 1992), a n d in their rates of maturation a n d d e s i c c a t i o n (Claridge et  al.  1993b; J o h n s o n  Elaphomyces  granulatus  1994a). (described  F o r e x a m p l e , the  common  and  widespread  by Smith et al. 1981) often fruits prolifically a n d  g e n e r a t e s long-lasting truffles that are s l o w to mature a n d persist in the substrate  25 year-round  (Hunt a n d T r a p p e 1987; L u o m a et al.  1 9 9 1 ; J o h n s o n 1994a).  In  contrast, s e v e r a l u n c o m m o n to rare m e m b e r s of the B a s i d i o m y c e t e s often fruit every few y e a r s during a particular s e a s o n a n d tend to p r o d u c e a scattering of e p h e m e r a l fleshy truffles that d e v e l o p rapidly but last only a few w e e k s before ( C a s t e l l a n o et al. 1989).  decaying  Hunt a n d T r a p p e (1987) h y p o t h e s i z e that differences in  fruiting patterns b e t w e e n truffle s p e c i e s m a y be partly d u e to differences in their temperature a n d moisture thresholds, optimum metabolic temperatures, a n d the e n e r g y or nutrient storage capability of the m y c e l i u m . Variability  in the  production  and  species composition  of truffles  during  concurrent s a m p l i n g b e t w e e n sites h a s b e e n a s s o c i a t e d with differences in stand a g e , stand structure, forest c o m p o s i t i o n , a n d disturbance history (Last et al. 1979; V o g t et al.  1 9 8 1 ; Dighton et al.  1986; L u o m a et al.  1 9 9 1 ; O ' D e l l et al.  1992;  A m a r a n t h u s et al. 1994; C l a r k s o n a n d Mills 1994; W a t e r s et al. 1994; North et al. 1997; S t a t e s a n d G a u d 1997).  Underlying differences in habitat conditions a n d  r e s o u r c e s a m o n g t h e s e stand types m a y explain the differences s e e n in truffle c o m m u n i t i e s b e t w e e n s u c h s t a n d s ( J o h n s o n 1 9 9 4 a ; C l a r i d g e et al. 2 0 0 0 b ) .  Truffle communities in the Pacific Northwest A n u m b e r of truffle s p e c i e s h a v e b e e n found during s y s t e m a t i c s a m p l i n g in the Pacific Northwest (Table 3). L u o m a et al. (1991) collected the most s p e c i e s (47) during a 4 8 - m o n t h study in 10 Douglas-fir (Pseudotsuga  menziesii  (Mirb.) F r a n c o )  s t a n d s of a range of a g e s (young, mature, old-growth) a n d moisture c l a s s e s (wet, m e s i c , dry).  In multi-year studies, s o m e truffle s p e c i e s (by weight or  number)  d o m i n a t e d every y e a r while others did not (Fogel 1976; Hunt a n d T r a p p e 1987). Production of truffles per y e a r varies b e t w e e n a r e a s , e v e n after correcting  for  26 T a b l e 3.  S u m m a r y of the n u m b e r of t a x a , density, a n d standing crop of truffles collected in published studies from the P a c i f i c Northwest. V a l u e s are taken directly from, calculated from, or estimated (~) using tables or g r a p h s in the citation.  Standing crop Duration and ecosystem 36 months; Douglas-fir forest in western O r e g o n 13 months; Douglas-fir forest in w e s t e r n O r e g o n 6 months; Pacific silver fir forests in western Washington 32 months; Douglas-fir forest in western O r e g o n 4 8 months; Douglas-fir forests in O r e g o n  Stand type & age (years) (40 to 65)  (35 to 50)  young (23) mature (180) (35 to 50)  young (<80) mature (80 to 199)  Number of taxa a  Truffle density (no. ha )  ( 9 site session  1  k  1  16 g e n e r a , 24 s p . (3 8 major) 15 s p .  11,052 16,753  < 9.6  —  1 sp.  —  2 months; Douglas-fir forests in southwest Oregon 12 months; white fir forests in northeastern California  ) site' year  1  1  1  Reference Fogel (1976)  0-10  2.35.4 (43.9) (24.0)  —  (1)  V o g t er al. (1981)  < 142  (380)  Fogel and Hunt (1979)  11 g e n e r a , 30 s p . (4 7 major)  5,8156,648  0.1517.51  2.03.2 (35.4)  Hunt a n d Trappe (1987)  4 7 s p . (5 7 major)  -2000  <9.9  1.2  C  2.2  C  Luoma (1991); L u o m a et al. (1991)  old-growth (>200) 10 months; Douglas-fir forests in O r e g o n  h a  0.7^.6 c  clearcut plantations (4 to 27)  8 s p . out of 21 s p .  100300  £0.14  0.07  mature (180) clearcuts (< 28) forest remnants heavy thinned moderately thinned mature controls (70 to 99)  18 s p . out of 21 s p . absent  3,20016,000  <6.4  3.5  —  —  —  12 g e n e r a  6,029  8.8  8.8  14 g e n e r a  —  £7.18  1.995.16 1.273.28 1.21 1.41'  c  Amaranthus etal. (1994)  C  Clarkson & Mills (1994)  c  e  W a t e r s et al. (1994)  27 Table 3.  (continued)  Duration and ecosystem 2 months; fir forests in California  46 months; western hemlock forests in Washington  Stand type & age (years) young (75 to 95) shelterwood old-growth (> 200) managedyoung naturalmature old-growth (> 300)  24 months; fir forests in California  mature (100) old-growth (> 200)  Number of taxa 3  Truffle density (no. ha ) 1  Standing (kg ha site' session 1  1  crop ) site' year  1  b  1 1  Reference  Reported mean frequency ofsporocarps in plots (%): 4.2% (shelterwood) to 27.8% (old-growth)  Waters and Zabel (1995)  27 sp. out of 43 sp. (1 major) 29 sp. out of 43 sp. (1 major) 34 sp. out of 43 sp. (1 major) 38 sp. out of 46 sp. (3 major) 38 sp. out of 46 sp. (3 major) 4 major genera  North et al. (1997)  3,135  -0.51.2  0.78  -3.56.5  4.51  -2.84.7 < 27.47 -0.2-7.5  4.02  2.43  Waters et al. (1997)  -1.0-4.5  9 months; (110 to 130) 2.7Cazares et Douglas-fir 6.1 al. (1999) forests in Oregon 33 months; thinned < 11.1 Colgan et 46 sp. 1,213 0.23 Douglas-fir (55 to 65) (11 major) al. (1999) forests in control 0.49 Washington (55 - 65) major species are those that represent at least 5% of the total biomass or total number of truffles within a specified time or habitat (Hering 1966 and subsequently used by others, e.g. Fogel 1976; Vogt et al. 1981; Hunt and Trappe 1987; Luoma etal. 1991; Colgan etal. 1999). 'Two approaches were used to calculate standing crops (described by Hunt and Trappe 1987): 1) standing crops (kg per ha) were determined for each sampling period and then summed for the year (values inside parentheses), or 2) the biomass and area sampled within the year was accumulated for one conversion at year end (values outside parentheses). Standing crops are expressed as mean values across stand types. a  c  28 different methods of calculation. However, comparisons of numbers of species or production of truffles among studies must keep in mind the duration and intensity of sampling and the methods of truffle collection and estimations of productivity. Although mycorrhizae of some hypogeous species have been studied (e.g. Sakakibara et al. 2002) and some truffle collecting has occurred (Harrison and Smith 1968) in B.C., there has been no published study that systematically examines the occurrence and abundance of truffles in B.C. forests. Furthermore, most previous studies of truffle communities in the Pacific Northwest have been in Douglas-fir stands (Table 3); relatively little is known about truffle communities in forests dominated by western hemlock, which are more common in coastal B.C. Carey (1991, 1995) suggests that western hemlock forests may have a lower diversity and abundance of truffles compared to Douglas-fir forests, possibly because western hemlock have fewer known mycorrhizal associates (>50 species, Kropp and Trappe 1982) than do Douglas-fir (>2,000 species, reviewed in Bruns 1995). Although North et al. (1997) found 43 truffle species in western hemlock forests in Washington, one species (Elaphomyces  granulatus) dominated, representing 92.8% of the total  standing crop.  Truffles and flying squirrels - is there a relationship? Why are the average densities of northern flying squirrel populations higher in some habitats than others? The factors responsible for these differences have been the subject of intense study and continuing debate.  This question is particularly  relevant because of its management implications (Krebs 2002); by manipulating the primary factor that limits populations of northern flying squirrels, their numbers can be increased. Such increases in the prey base could enable managers to improve  29 the quality of foraging habitat for northern spotted owls (Ransome 2001, 2004). Any factor that affects movements or survival of individuals can limit animal populations through its effect on immigration, emigration, birth rates or death rates (Sinclair 1989; Krebs 2002). Krebs (2002) lists six factors that can limit the size of animal populations: nest sites, food, predation, disease/parasites, weather conditions, and behavioural responses (e.g. territoriality). The effect of nest sites and food has been examined to some degree for northern flying squirrel populations (described below).  Several authors have suggested that populations of northern flying squirrels are primarily limited by the abundance of tree cavities for den sites (Volts 1986; Carey 1991; Carey et al. 1992, 1995, 1997). This conclusion was based on a positive correlation between either the number of tree cavities (Carey et al. 1992) or the density of dead standing trees (Volts 1986; Carey 1995) and the abundance of northern flying squirrels. However, these findings were not consistent with other studies in which no correlation was found between the abundance or density of northern flying squirrels and the density of tree cavities (Waters and Zabel 1995) or dead standing trees (Rosenberg and Anthony 1992; Waters and Zabel 1995). Furthermore, many studies have documented northern flying squirrels constructing and using outside nests or drays (Cowan 1936; Weigl and Osgood 1974; Mowrey and Zasada 1984; Carey et al. 1997). In addition, populations of northern flying squirrels did not increase following the addition of nest boxes in coastal British Columbia (Ransome and Sullivan 2004) and in Washington (Colgan 1997; Carey 2002), even though flying squirrels readily used these structures (Maser et al. 1981; Harestad 1990; Carey 2002; Ransome and Sullivan 2004). This suggests that factor(s) other than the abundance of cavities limited populations of flying squirrels  30 at t h e s e sites. T h e availability of natural food in a n a r e a m a y limit the density of  northern  flying squirrels ( R o s e n b e r g a n d A n t h o n y 1 9 9 2 ; W a t e r s a n d Z a b e l 1995; R a n s o m e a n d Sullivan 1997).  W a t e r s a n d Z a b e l (1995) reported a correlation b e t w e e n the  density of northern flying squirrels a n d the f r e q u e n c y of plots containing at least o n e truffle.  In a food supplementation experiment in l o d g e p o l e pine (Pinus  contorta  Dougl.) s t a n d s in the south-central interior of British C o l u m b i a , populations northern  flying  squirrels  i n c r e a s e d following  ( R a n s o m e a n d Sullivan 1997).  the  addition  of  sunflower  of  seeds  F o o d s u p p l e m e n t a t i o n using sunflower s e e d s a l s o  i n c r e a s e d the density of t o w n s e n d ' s c h i p m u n k s {Tamias townsendii  Bachman)  (Sullivan et al. 1983), red squirrels (Sullivan 1990; K l e n n e r a n d K r e b s 1991) a n d D o u g l a s squirrels (T. douglasii B a c h m a n ) (Sullivan a n d Sullivan 1982). In m a n a g e d s t a n d s , North et al. (1997) s u g g e s t that truffle a b u n d a n c e is most limiting  for  m y c o p h a g i s t s in winter, w h e n the standing crop of truffles is lowest a n d c o n s u m p t i o n c a n e x c e e d availability (North et al. 1997).  OBJECTIVES: T h i s study investigated the relationship b e t w e e n populations of truffles a n d northern flying squirrels in five coniferous forests in c o a s t a l B . C .  I a d d r e s s e d the  following q u e s t i o n s :  1)  What is the occurrence and abundance of truffle species at each site? T h e r e is a r e m a r k a b l e dearth of information on s p e c i e s r i c h n e s s a n d productivity of truffles in forests of B . C . In addition to improving our understanding of truffle c o m m u n i t i e s in c o a s t a l forests d o m i n a t e d by w e s t e r n h e m l o c k , s y s t e m a t i c  31 s a m p l i n g of truffle populations from  e a c h site provided  a n index of  the  a b u n d a n c e of food r e s o u r c e s for northern flying squirrels, w h i c h w a s integral in a d d r e s s i n g the following objectives.  2)  How important are truffles in the year-round diet of northern flying squirrels? In m a n y studies, truffles represent a significant food item in the diet of  northern  flying  squirrels.  However,  if western  hemlock  forests  have  d e p a u p a r a t e truffle c o m m u n i t i e s a s s u g g e s t e d by C a r e y ( 1 9 9 1 , 1995), northern flying squirrels inhabiting s u c h s t a n d s m a y not be a s d e p e n d e n t o n this fungal food s o u r c e a s h a s b e e n d o c u m e n t e d in other forest types.  In m o s t studies,  populations of northern flying squirrels have b e e n s a m p l e d twice yearly, usually in the spring a n d fall (e.g. C a r e y 1995; C o l g a n 1997; C a r e y et al. 1999, 2 0 0 2 ; C a z a r e s et al. 1999; P y a r e a n d L o n g l a n d 2 0 0 1 a ; Mitchell 2001), which limits descriptions of their diet to t h e s e times. In this study, squirrels w e r e live-trapped year-round, providing a more c o m p l e t e picture of their diet.  3) Which truffle taxa do northern flying squirrels select for consumption? Despite n u m e r o u s studies describing the diet of northern flying squirrels, prior to the initiation of this r e s e a r c h , there had b e e n no p u b l i s h e d studies e x a m i n i n g the c o n s u m p t i o n of truffles in relation the availability of this f o o d o n a site. S u c h a n a p p r o a c h is n e e d e d to fully understand the food habits of a n i m a l s ( M c K e e v e r 1960; Batzli a n d C o l e 1979; J o h n s o n 1994b; C o l g a n 1997) a n d to differences in diets, if any, b e t w e e n localities ( M a s e r et al. 1985).  interpret  Managing  s t a n d s to promote prey populations of northern spotted owls is a i d e d by a n  32  understanding of the important food items in the diet of northern flying squirrels and the taxa of truffles that are targeted for consumption by squirrels.  4)  Is the density of resident northern flying squirrels positively correlated  with truffle production on a site? This research provides a year-round study of the relationship between flying squirrels and truffles at five sites. This approach improves on the work of Waters and Zabel (1995), who sampled truffles over a two-month period.  33 MATERIALS AND METHODS  Study areas T h e study a r e a s w e r e in five w a t e r s h e d s in southwestern British C o l u m b i a , C a n a d a , n e a r the city of V a n c o u v e r (Figure 1). A 3 2 - h a site w a s s e l e c t e d within e a c h of the C a p i l a n o w a t e r s h e d ( C A P , 49° 2 7 ' 3 3 " N 123° 06' 3 2 W ) , S e y m o u r Demonstration  Forest ( S D F , 49° 15' 5 3 " N 122° 3 3 ' 3 6 W ) , C o q u i t l a m  watershed  ( C O Q , 49° 2 1 ' 19"N 122° 4 5 ' 5 2 " W ) , M a l c o l m K n a p p R e s e a r c h F o r e s t ( R e s e a r c h F o r e s t or R F , 49° 2 2 ' 2 4 " N 123° 0 0 ' 2 9 " W ) a n d C h e h a l i s w a t e r s h e d ( C H E H , 4 9 ° 19' 5 2 " N 121° 5 9 ' 3 3 " W ) . T h e s e sites a l s o s e r v e d a s controls in the experimental d e s i g n of a larger related study ( R a n s o m e 2 0 0 1 ; R a n s o m e a n d Sullivan 2 0 0 2 , 2 0 0 3 , 2004). A l l sites are within the C o a s t a l W e s t e r n H e m l o c k ( C W H ) biogeoclimatic z o n e ; the C a p i l a n o , C o q u i t l a m , and C h e h a l i s sites are in the very wet maritime s u b z o n e ( C W H v m ) a n d the R e s e a r c h F o r e s t a n d S e y m o u r D e m o n s t r a t i o n F o r e s t sites a r e in the dry maritime s u b z o n e ( C W H d m ) ( G r e e n a n d Klinka 1994).  T h e climate in this  z o n e is moderate, with c o o l s u m m e r s and mild winters (Meidinger a n d P o j a r 1991). M e a n a n n u a l precipitation is 2,787 m m in the C W H v m s u b z o n e a n d 1,827 m m in the C W H d m s u b z o n e (Meidinger a n d Pojar 1991), a n d falls mostly a s rain ( G r e e n a n d Klinka 1994). M e a n a n n u a l temperature is 8.2°C in the C W H v m s u b z o n e a n d 9.8°C in the C W H d m s u b z o n e (Meidinger a n d Pojar 1991). T o p o g r a p h y includes flat, gently rolling, a n d moderately s l o p e d terrain a n d elevations range from 160 to 4 0 0 masl. C a n d i d a t e sites initially w e r e identified from forest c o v e r m a p s in e v e n - a g e d s e c o n d growth (60- to 70-year-old; R a n s o m e 2001) forests. be  as  similar  as  possible,  matching  stand  attributes  S i t e s w e r e s e l e c t e d to such  as  tree  species  F i g u r e 1.  L o c a t i o n of five study sites s a m p l e d for truffles a n d northern flying squirrels in 1997 a n d 1998.  34  35 c o m p o s i t i o n , a g e c l a s s , height c l a s s (at least 28.5-m), site c l a s s (good), a n d crown c l o s u r e (66 - 7 5 % ) . S i t e s w e r e a l s o a c c e s s i b l e by road a n d large e n o u g h to fit a trapping grid (12.8 ha) a n d additional buffer strip of similar forest at least 100-m w i d e (for a total a r e a of c a . 32 ha). T h e suitability of e a c h site w a s c h e c k e d during a s u b s e q u e n t field a s s e s s m e n t .  B e c a u s e s t a n d s w e r e not randomly p i c k e d , a n y  inferences b e y o n d the study sites s h o u l d b e m a d e with caution. T h e overstory at all sites w a s d o m i n a t e d by coniferous s p e c i e s , including w e s t e r n h e m l o c k a n d western r e d c e d a r (Thuja plicata Donn), with l e s s e r a m o u n t s of Douglas-fir a n d P a c i f i c silver fir (Abies amabilis Dougl.) (Table 4).  M e a n diameter at  breast height (dbh) of all tree s p e c i e s s a m p l e d at e a c h site ranged from 30.7 c m in C a p i l a n o to 3 9 . 0 c m in the S e y m o u r Demonstration Forest (Table 5).  Deciduous  overstory s p e c i e s included red alder (Alnus rubra Bong.), black cottonwood (Populus balsamifera B r a y s h a w ) , a n d big-leaf m a p l e (Acer macrophyllum w a s d o m i n a t e d by O r e g o n b e a k e d m o s s (Kindbergia m o s s (Hylocomium (Plagiothecium  splendens  undulatum  Pursh). Vegetation  oregana (Sull.) O c h y r a ) , step  (Hedw.) S c h i m p . ) , a n d w a v y - l e a v e d cotton m o s s  (Hedw.)  huckleberry (Vaccinium parvifolium  Schimp.),  with  varying  S m . ) , sword fern (Polystichum  amounts  of  red  munitum (Kaulf.)  Presl.), a n d s a l a l (Gaultheria shallon P u r s h ) . E a c h site w a s naturally regenerated following clear-cut logging a n d burning in the 1 9 2 0 s a n d 1 9 3 0 s . T h e R e s e a r c h Forest site w a s burned in a n e x t e n s i v e fire in 1931 (Klinka a n d Krajina 1986). T w o intense b u s h fires a l s o burned at the S e y m o u r Demonstration F o r e s t site in 1 9 1 0 a n d 1921 (Kahrer 1989).  F e w old-growth  l e g a c i e s , s u c h a s large d i a m e t e r veteran trees (live or d e a d ) a n d d o w n e d w o o d , r e m a i n e d within all s t a n d s ( R a n s o m e 2001). Within e a c h study a r e a , a rectangular 12.8-ha grid w a s e s t a b l i s h e d in a n  36  T a b l e 4.  M e a n density (trees/ha) ± S E of the four m a i n tree s p e c i e s a n d all tree s p e c i e s at the five sites (N = 20).  Western hemlock  Western redcedar  CAP  4 4 3 ± 59  CHEH  Douglas-fir  Pacific silver fir  Total  185 ± 3 9  33 ± 9  130 ± 3 7  780 ± 6 0  240 ± 6 2  295 ± 40  23 ± 9  ~  6 4 8 ± 52  COQ  130 ± 2 1  2 3 8 ± 31  85 ± 2 5  8±4  468 ± 44  RF  132 ± 2 0  447 ± 46  55 ± 15  ~  684 ± 51  SDF  273 ± 42  125 ± 2 7  120 ± 2 8  —  535 ± 4 9  Site  i n c l u d e s all live trees e n c o u n t e r e d in twenty 2 0 0 - m plots/grid systematically located (every 50-m) a l o n g transects 1 0 0 - m apart. S E = s t a n d a r d error of the m e a n i!  T a b l e 5.  with  3  plots  M e a n d i a m e t e r s at breast height (cm) ± S E of the four m a i n tree s p e c i e s and all tree s p e c i e s at the five sites (N = 20).  Western hemlock  Western redcedar  Douglas-fir  Pacific silver fir  Total  CAP  31.3 ± 1.1  31.9 ± 1.3  35.9 ± 6 . 2  26.8 ± 1.8  30.7 ± 1.0  CHEH  33.5 ± 1.1  36.4 ± 1.6  60.4 ± 10.2  —  35.2 ± 1.0  COQ  30.2 ± 2 . 2  34.6 ± 2 . 5  49.4 ± 5.2  20.4 ± 3.0  35.3 ± 1.6  RF  31.9 ± 1.9  32.0 ± 1.7  57.2 ± 3 . 1  —  34.1 ± 1.2  SDF  34.0 ± 2.2  38.5 ± 5 . 1  53.3 ± 1.7  —  39.0 ± 1.7  Site  i n c l u d e s all live trees e n c o u n t e r e d in twenty 200-rn^ plots/grid s y s t e m a t i c a l l y located (every 50-m) a l o n g transects 1 0 0 - m apart. S E = s t a n d a r d error of the m e a n  with  3  plots  37 8 x 1 0 s y s t e m a t i c layout with 4 0 - m s p a c i n g b e t w e e n stations. T h i s grid w a s u s e d a s a f r a m e of reference for locating fungal s a m p l e plots, habitat t r a n s e c t s , a n d livetrapping station points {described below).  Sampling and identification of truffles S e v e r a l authors h a v e highlighted the c h a l l e n g e s involved in s a m p l i n g truffles, specifically in determining a n a d e q u a t e plot layout, plot s h a p e a n d s i z e , a n d total s a m p l i n g a r e a to obtain a representative stand s a m p l e (e.g. F o g e l a n d Hunt 1979; Hunt a n d T r a p p e 1 9 8 7 ; L u o m a et al. 1991).  V a r i a t i o n in the fruiting patterns of  s p e c i e s within a n d b e t w e e n y e a r s c a n c o m p l i c a t e attempts  to estimate  truffle  production ( F o g e l 1976; Hunt a n d T r a p p e 1987; L u o m a et al. 1991) a n d d o c u m e n t the s p e c i e s that o c c u r (Hunt a n d T r a p p e 1987; V o g t et al. 1992; C o l g a n et al. 1999) in a n a r e a . T h e c l u m p e d distribution of individual fruitbodies (Fogel 1 9 7 6 , 1 9 8 1 ; States  1 9 8 5 ; V o g t et al. 1992) m a k e s s a m p l i n g m a n y d i s p e r s e d s m a l l  plots  preferable to s a m p l i n g fewer a g g r e g a t e d large plots ( L u o m a et al. 1 9 9 1 ; North et al. 1997). Truffle production at the stand level c a n b e overestimated if s a m p l e plots a r e too large, t o o few, or t o o aggregated o n a site (Hunt a n d T r a p p e 1987; L u o m a et al. 1991). S a m p l i n g a n d identification  of truffles c a n b e labour intensive a n d time  c o n s u m i n g ( F o g e l 1976; V o g t et al. 1 9 8 1 ; Hunt a n d T r a p p e 1987; C l a r i d g e et al. 1993b; J o h n s o n 1994a).  D e p e n d i n g o n microhabitat conditions, o n e 4 - m plot c a n 2  take up to 6 p e r s o n hours (this study) or 8 p e r s o n hours (Vogt et al. 1981) to fully e x c a v a t e , a n d in extreme c a s e s c a n yield h u n d r e d s of truffles (e.g. L u o m a 1 9 9 1 ; this study) to p r o c e s s a n d identify in the lab. Ideally, the duration of e a c h s a m p l i n g s e s s i o n s h o u l d b e c o n d e n s e d a s m u c h a s p o s s i b l e to better e q u a l i z e the conditions  38 that influence truffle fruiting (such a s temperature a n d moisture) b e t w e e n the study sites ( L u o m a et al. 1991).  Declining daylight hours in the fall a n d winter months  i m p o s e further restrictions on the time available for s a m p l i n g e a c h site during a session.  Practical limitations on the n u m b e r of s a m p l e plots that c a n be c o m p l e t e d  during a s e s s i o n a n d the n u m b e r of s e s s i o n s that c a n be c o m p l e t e d throughout the y e a r are therefore inevitable (Fogel 1981).  A b a l a n c e must be struck b e t w e e n a  s a m p l e d a r e a large e n o u g h to a d e q u a t e l y quantify the a n n u a l production of truffles given the areal extent of the site to be represented (Hunt a n d T r a p p e 1987), a n d a s m a l l e n o u g h s a m p l e s i z e to minimize the potential impacts to the forest e c o s y s t e m (Vogt et al. 1 9 9 2 ; C l a r i d g e et al. 1993b) a n d the c o s t s a n d time a s s o c i a t e d with the s a m p l e (Hunt a n d T r a p p e 1987). Ultimately, what c a n be a c c o m p l i s h e d will d e p e n d on the specific objectives of the study, the n u m b e r of study a r e a s , the s i z e of e a c h site, a n d the budget allocated for the project. Following r e c o m m e n d a t i o n s outlined in Hunt a n d T r a p p e (1987), I m a x i m i z e d the f r e q u e n c y a n d intensity of s a m p l i n g for truffles on e a c h site a s m u c h a s w a s feasible given our time constraints a n d limited budget.  E a c h site w a s s a m p l e d over  a two- to three-week period up to nine times (or ' s e s s i o n s ' ) from M a y 1997 to F e b r u a r y 1999 ( T a b l e s 6 a n d 7).  S a m p l i n g o c c u r r e d at three to five sites during  e a c h s e s s i o n from M a y 1997 to F e b r u a r y 1998; e a c h site w a s visited o n e to four times during this period (Table 6).  T h e s a m p l i n g m e t h o d o l o g y w a s modified in  F e b r u a r y 1998; all five sites w e r e consistently s a m p l e d four times at  10-week  intervals from April 1998 to D e c e m b e r 1998 (hereafter referred to a s the primary collection period; T a b l e 7). I s a m p l e d twenty-four 4 - m  2  circular (1.13-m radius) plots at e a c h site during  the first two s e s s i o n s (Table 6) a n d thirty-two 4 - m circular plots at e a c h site during 2  39 T a b l e 6.  Truffle s a m p l i n g s c h e d u l e at the five sites during the four s e s s i o n s in 1997 a n d early 1998, prior to i m p r o v e m e n t s in the s a m p l i n g methodology.  Total area sampled (m )  Sampling Session (1997, early 1998) Site CAP  N o . of plots: Dates (mo/day):  CHEH  No. of plots: Dates (mo/day):  COQ  N o . of plots: Dates (mo/day):  RF  N o . of plots: Dates (mo/day):  SDF  Late Spring  Late Summer  Late Fall  24  24  14  32  05/23 06/07  09/08 09/16  11/2412/02  02/1002/12  3  3  24  32  06/09 06/10  11/2711/28  6  32  25  06/05  09/01 09/04  11/21 12/15  02/23 02/24  24  24  32  29  06/04  08/25 09/06  12/03  02/1702/20  32  2  11/2012/01  02/26  142  88  96  72  2  376  224  24  N o . of plots:  No. of plots:  Winter  24  Dates (mo/day): Total  3  -  420  436  136  1,592 Dates 05/23 08/25 11/2002/10(mo/day): 06/10 09/16 12/15 02/26 ao iS a m p l i n g w a s c a n c e l e d or only partially c o m p l e t e d on s o m e sites d u e to time a n d budget constraints or s n o w conditions. ^ S a m p l i n g w a s c a n c e l e d or only partially c o m p l e t e d o n s o m e sites d u e to a c h a n g e in the s a m p l i n g methodology mid-way through this s e s s i o n . a  40 T a b l e 7.  Truffle s a m p l i n g s c h e d u l e at the five sites during the primary collection period in 1998 a n d 1 c a n c e l e d s e s s i o n in 1999, following i m p r o v e m e n t s in the s a m p l i n g methodology.  Sampling Session (1998, early 1999) Site CAP  N o . of plots: Dates (mo/day):  CHEH  No. of plots: Dates (mo/day):  COQ  No. of plots: Dates (mo/day):  RF  N o . of plots: Dates (mo/day):  SDF  N o . of plots: Dates (mo/day):  Total  N o . of plots:  Spring  Summer  Early Fall  Late Fall  32  32  32  32°  04/27 05/01  07/02 07/15  09/1509/27  12/0812/17  32  32  32  24  3  Winter  6  02/01  480  12/11 12/13  07/08  09/13  32  32  32  26  04/23 04/24  07/16  09/1809/22  12/1612/18  32  32  32  32  24  04/20 04/24  07/06 07/10  09/1009/14  12/0412/10  01/31 02/05  32  32  32  32  28  04/21 04/22  06/29 07/17  11/21 12/19  01/3002/07  160  160  146  52  160  2  512  05/01  09/11 09/16  Total area sampled (m )  488  608  624  2,712 Dates 04/20 06/29 11/21 09/1001/31 (mo/day): 05/01 07/17 09/27 12/19 02/07 'Sampling w a s c a n c e l e d or only partially c o m p l e t e d on s o m e sites d u e to time constraints and/or s n o w conditions. T h e winter s a m p l i n g s e s s i o n w a s c a n c e l e d at three sites d u e to h e a v y snowfall a n d frozen ground conditions. ° S n o w c o v e r e d the ground during this s e s s i o n (5 to 30 c m of s n o w c o v e r within plots).  41 the remaining s e v e n ( T a b l e s 6 a n d 7) s e s s i o n s .  S o m e sites w e r e only partially  s a m p l e d d u e to time a n d budget constraints, c h a n g e s in m e t h o d o l o g y (February 1998), or s n o w conditions (e.g. F e b r u a r y 1999, T a b l e s 6 a n d 7). T h e 96 m  2  of e x c a v a t e d a r e a s a m p l e d in the late spring a n d late s u m m e r  1997 w a s slightly below the minimal a r e a of 100 m per s e s s i o n that F o g e l (1976) 2  recommended.  H o w e v e r , the 128 m a r e a s a m p l e d in e a c h of the remaining visits 2  s u r p a s s e d the a r e a s a m p l e d for truffles at a single site during a single s e s s i o n in all but o n e study from the P a c i f i c Northwest published to date ( W a t e r s a n d Z a b e l 1 9 9 5 ; T a b l e 8). T h e total a r e a s a m p l e d for truffles at e a c h site during the primary collection period ranged from 4 8 0 m  2  to 512 m , w h i c h is l e s s than ( F o g e l a n d Hunt 1979), 2  c o m p a r a b l e to (Fogel 1976; Hunt a n d T r a p p e 1987; North et al. 1997; W a t e r s et al. 1997; C o l g a n et al. 1999) or in e x c e s s of (Vogt et al. 1 9 8 1 ; L u o m a et al. 1 9 9 1 ; A m a r a n t h u s et al. 1994; C l a r k s o n a n d Mills 1994; W a t e r s et al. 1994; W a t e r s a n d Z a b e l 1995) the total a r e a s a m p l e d annually in other studies (Table 8). U s i n g the e s t a b l i s h e d live-trapping grid a s starting points, three a n d then four stations per grid-line w e r e randomly s e l e c t e d a n d plots w e r e p l a c e d on bare-ground sites in 'representative' a r e a s within 2 0 m of t h e s e stations.  B a r e - g r o u n d sites  e x c l u d e d tree s t e m s , intact logs (i.e. d e c a y c l a s s I to III; S t e v e n s 1997), large rocks, standing water, or a n y other non-truffle producing substrate (> 0.125 m wide) within the 4 - m plot. 2  ' R e p r e s e n t a t i v e ' a r e a s w e r e subjectively c h o s e n to reflect the overall  c o v e r a n d s p e c i e s c o m p o s i t i o n of vegetation a n d the g e n e r a l s l o p e a n d a s p e c t of the a r e a . B y April 1998, the s a m p l i n g a p p r o a c h had b e e n improved a n d plots w e r e instead p l a c e d at a pre-determined bearing a n d d i s t a n c e from four randomly c h o s e n stations per grid-line. Plots w e r e still p l a c e d on bare-ground a r e a s but w e r e m o v e d  T a b l e 8.  S u m m a r y of m e t h o d s u s e d to s a m p l e truffle populations in published studies from the Pacific Northwest during the past 30 y e a r s .  Ecosystem  Number of sites and stands  Sampling regime site" session' 1  1  Sampling interval and duration  Area sampled site' session" 1  1  Reference  100 m*  1,200 rrr*  F o g e l and Hunt (1979)  Monthly for 6 months, during the snow-free period  4 8 m*  288 m  V o g t et al. (1981)  - M o n t h l y for 2 years  4 8 nrr^  4 8 0 m* to 528 m  Hunt and Trappe (1987)  2 5 4-rrf plots systematically p l a c e d every 2 5 m along 3 transects  O n c e in spring and fall, o n c e in s u m m e r (in o l d growth stands) for 4 years  100 m*  200 m to 300 m  L u o m a et al. (1991)  15 pairs of 1-rn^ plots (on C W D and soil) systematically p l a c e d a l o n g 5 transects  4 s e s s i o n s over 10 months  30 m^(15 m in C W D , 15 m in soil substrates)  120 m^  Amaranthus etal. (1994)  50 m  1 1.2-ha stand  4 randomly located 5 x 5 m quadrats  Monthly for 1 y e a r  2 3 - a n d 180-year-old P a c i f i c silver fir forests in w e s t e r n Washington  1 site, 2 stands  12 randomly located 4 - m plots  3 5 - to 50-year-old Douglas-fir forest in western Oregon  1 1.5-ha stand  12 4-nrf plots  Y o u n g (< 80 y e a r s ) , mature ( 8 0 - 1 9 9 y e a r s ) , a n d old-growth (>200 y e a r s ) D o u g l a s fir forests in O r e g o n  1 site, 10 ~ 5-ha stands  C l e a r c u t plantations (4- to 27-year-old) and mature (180-year-old) Douglas-fir forests in Oregon  2 2.4-ha stands and 5 plantations  3 5 - to 50-year-old Douglas-fir forest in western Oregon  1  Fogel (1976)  Monthly for 3 years  1 20-ha stand  1  600 m  50 randomly located 1 - m plots (and 4 1 0 0 - m quadrats)  4 0 - to 65-year-old Douglas-fir forest in western Oregon  Area sampled site" year"  2  2  z  2  2  2  z  2  2  2  42  2  T a b l e 8.  (continued)  Number of sites and stands  Area sampled site" session"  Area sampled site year"  Sampling regime site' session"  Sampling interval and duration  24 to 4 0 1 - m plots within 5-m of a randomly c h o s e n trap stations (15-m spacing)  One summer s a m p l i n g from m i d J u n e to mid-August  24 m to 4 0 m  0.39-ha stands  using a 5 x 6 grid (8-m s p a c i n g )  plots ), early fall (15 plots) over 1 y e a r  120 m  1 site, 12 9 - h a to 13ha stands  91 to 104 4-rrC plots p l a c e d at e a c h live-trapping station (40-m spacing)  O n e s a m p l e in June/July  364 m to 416 m  364 m to 416 m  Waters and Zabel (1995)  Managed-young, natural-mature, a n d old-growth (> 3 0 0 year-old) w e s t e r n h e m l o c k forests in Washington  2 sites, 18 stands  11 4 - m a n d 1 6-m* plots, paired along a transect (open a n d under e x c l o s u r e s ) every 20 m  4 to 6 s e s s i o n s year" over 3.8 y e a r s  100 nT (50 m of o p e n sampling, 50 m of exclosure sampling)  4 0 0 m to 600 m  North et al. (1997)  O l d growth (> 2 0 0 year-old) a n d mature (~ 100-year-old) fir forests in California  4 sites, 8 0.25-ha stands  36 4 - m circular plots p l a c e d near grid points using a 6 x 6 grid (10-m spacing)  3 to 4 s e s s i o n s at monthly intervals during snow-free periods, over 2 years  144 m  432 m to 576 m  W a t e r s et al. (1997)  Ecosystem F o r e s t remnants a n d clearcuts in southwest Oregon  4 1.3-ha to 3.6-ha stands, 2 clearcuts  1  1  2  1  1  2  1  1  Reference  24 m to 40 m  Clarkson & Mills (1994)  z  2  A  old) white fir forests in northeastern California O l d (> 200-year-old), shelterwood, and y o u n g (75- to 95-yearold) fir forests in California  2  1  on r«2 al. (1994)  2  z  2  2  z  2  2  2  2  43  z  2  2  T a b l e 8.  (continued)  Ecosystem  Number of sites and stands  Sampling regime site" session" 1  1  Sampling interval and duration  Area sampled site" session" 1  1  Area sampled site" year' 1  1  200 m  Reference C a z a r e s et al. (1999)  1 1 0 - t o 130-year-old Douglas-fir forests in Oregon  2 sites, 6 stands  2 5 4 - m plots systematically p l a c e d e v e r y 6-m a l o n g transects  2 s e s s i o n s year" (October 1993 and J u n e 1994)  100 m  5 5 - to 65-year-old Douglas-fir forests in Washington  4 sites, 16 10.2-ha stands  10 to 30 4 - m * plots systematically p l a c e d e v e r y 10-m a l o n g transects  5 s e s s i o n s year" every 12 w e e k s over 33 months (12 s e s s i o n s total)  4 0 m*to 120 m  200 to 600 m  C o l g a n et al. (1999)  6 0 - to 70-year-old western hemlock forests in British Columbia  5 sites, 5 12.8-ha stands  32 4 - m ^ plots from randomly c h o s e n trap stations, 4 per line.  4 times every 10 w e e k s (1998)  128 m  480 m* to 512 m  T h i s study  2  1  1  44  2  2  z  2  2  2  45 a s required a c c o r d i n g to rules e s t a b l i s h e d a priori. Interspersion of four starting points a l o n g e a c h of eight t r a n s e c t s in the livetrapping grid allowed plots to be more spatially distributed throughout e a c h site. E m p l o y i n g strict randomization to locate plots m a y result in truffle collections from only o n e part of the s t a n d ( s e e Hurlbert 1984). A n inter-plot d i s t a n c e of at least 4 0 m maintained i n d e p e n d e n c e of adjacent plots, a n d w a s e q u a l to ( W a t e r s a n d Z a b e l 1995) or more widely distributed than the s p a c i n g u s e d by other r e s e a r c h e r s (Table 8).  S a m p l i n g truffles within 4 - m circular plots is a s t a n d a r d i z e d m e t h o d (Table 8), 2  a n d facilitates c o m p a r i s o n s of results from different locations (Hunt a n d T r a p p e 1987). U s i n g objective rules to locate s a m p l i n g plots r e m o v e d the opportunity  for  o b s e r v e r s to be subjective in their plot p l a c e m e n t , w h i c h could potentially bias the results (Krebs 1999). Truffles w e r e collected from plots using m e t h o d s outlined by Hunt a n d T r a p p e (1987), C a s t e l l a n o et al. (1989), a n d L u o m a et al. (1991).  S e c o t i o i d fungi, w h i c h  often form s u b h y p o g e o u s fruitbodies at or near the substrate s u r f a c e , w e r e a l s o included in truffle collections, consistent with C a s t e l l a n o et al. (1989) a n d W a t e r s et al. (1997). Prior to e x c a v a t i o n , details that might prove useful in s u b s e q u e n t s p e c i e s identification, s u c h a s the a s s o c i a t e d plant a n d adjacent tree s p e c i e s , w e r e recorded ( C a s t e l l a n o et al. 1989). T h e s l o p e , a s p e c t , plot location, a n d s a m p l i n g date w e r e also recorded.  T h e n u m b e r of squirrel diggings on e a c h plot w a s noted a s a  p o s s i b l e index of m y c o p h a g y in the s a m p l e d a r e a .  W e then raked a n d carefully  hand-sifted through the organic layer a n d top 5 to 10 c m of mineral soil to extract the truffles present in a plot  (Hunt a n d T r a p p e 1987; C a s t e l l a n o et al. 1989; L u o m a et  al. 1991) a n d recorded the total time required to e x c a v a t e e a c h 4 - m  2  area.  Truffles w e r e counted a n d p l a c e d in labeled p a p e r b a g s , w h i c h w e r e then  46 w r a p p e d in w a x e d paper. T h e fresh fruitbody characteristics a n d fruiting substrate w e r e d e s c r i b e d a s a further aid in s p e c i e s identification ( C a s t e l l a n o et al. 1989). S i n c e this e x c a v a t i o n disturbed the top organic a n d soil layers, fine root structures, a n d fungal m y c e l i u m , plots w e r e s a m p l e d without r e p l a c e m e n t ( F o g e l 1976; Hunt a n d T r a p p e 1987) a n d sites w e r e m a r k e d with b i o d e g r a d a b l e flagging tape to avoid re-sampling any a r e a . In the laboratory, truffles w e r e stored in the refrigerator ( C a s t e l l a n o et al. 1989; W a t e r s et al. 1994) until p r o c e s s i n g for s p e c i e s identification.  Truffles w e r e  c l e a r e d of a n y adhering organic matter or soil, cut in half, a n d p l a c e d on racks to airdry ( W a t e r s et al. 1994).  O n c e dried, e a c h s p o r o c a r p w a s w e i g h e d to the nearest  0.01 g a n d p l a c e d in individually m a r k e d e n v e l o p e s . C o l l e c t i o n s w e r e identified to g e n u s (1997, early 1998) a n d to s p e c i e s (1998) through m i c r o s c o p i c e x a m i n a t i o n of s p o r o c a r p a n d s p o r e characteristics using k e y s a n d descriptions from D a n i e l s o n (1979), T r a p p e (1979), a n d C a s t e l l a n o etal. (1989).  Estimating standing crops and annual production of truffles Both the standing crop a n d percent f r e q u e n c y of e a c h truffle s p e c i e s a n d of all s p e c i e s c o m b i n e d w e r e determined for e a c h s e s s i o n a n d site.  Standing crops  w e r e calculated by s u m m i n g the e x c a v a t e d plot a r e a s a n d plot v a l u e s (grams dry weight a n d n u m b e r s of truffles collected) a n d then standardizing to a per hectare b a s i s (e.g. kg per h a a n d n u m b e r s of truffles per hectare) ( F o g e l 1976; Hunt a n d T r a p p e 1987). P e r c e n t f r e q u e n c i e s w e r e calculated by recording the p e r c e n t a g e of total plots with at least o n e detectable truffle. S t a n d i n g c r o p s provided a m e a s u r e of the a b u n d a n c e of the truffle food  r e s o u r c e ; percent f r e q u e n c i e s reflected  the  regularity of distribution of this food s o u r c e ( F o g e l a n d T r a p p e 1978; L u o m a et al.  47 1 9 9 1 ; C o l g a n 1997).  V a l u e s derived from sites with l e s s than 2 4 truffle plots p e r  s e s s i o n w e r e not included in further a n a l y s e s . Locating truffle plots o n only bare-ground sites {described above) m a x i m i z e d efficiency, allowing for the greatest a m o u n t of potential truffle substrate to b e s a m p l e d p e r unit effort a n d time. H o w e v e r , this a p p r o a c h n e c e s s i t a t e d adjusting the standing crop v a l u e s to a c c o u n t for a n y differences in the a r e a of bare ground p e r hectare at e a c h site.  T o estimate the a m o u n t of bare ground at e a c h site, t e n  approximately 3 0 0 - m long transects w e r e systematically located a c r o s s the s l o p e every 4 0 m a n d all objects (i.e. non-truffle producing c o m p o n e n t s ) intersecting the line w e r e m e a s u r e d along the ground to the nearest 0.25 m. A hip c h a i n (regularly tied off to r e d u c e stretch) w a s u s e d to record the total line d i s t a n c e of e a c h transect. Lengths along e a c h line that w e r e o c c u p i e d by objects w e r e s u m m e d , converted to a proportion of the total length, a n d a v e r a g e d a c r o s s all t r a n s e c t s (N=10). T h i s v a l u e w a s then u s e d to correct the standing c r o p s at e a c h site (corrected standing crop = [(100 - estimate of m e a n percent of o c c u p i e d ground per site) x kg p e r h a or n u m b e r of truffles per ha]). Indices of the a n n u a l production (truffle a b u n d a n c e ) a n d percent f r e q u e n c y (truffle o c c u r r e n c e ) from e a c h site w e r e determined using results from the primary collection period, which w a s the m o s t consistently a n d rigourously s a m p l e d , thus providing the best index. T h e standing crop v a l u e s (truffle b i o m a s s or n u m b e r s p e r hectare) e n c o u n t e r e d in e a c h stand during the primary collection period w e r e a v e r a g e d for the y e a r (equivalent to 'method 2 ' in Hunt a n d T r a p p e 1987).  A  correction factor to a c c o u n t for differences in a m o u n t of bare ground a r e a b e t w e e n sites w a s then a p p l i e d . O v e r a l l percent f r e q u e n c y of truffles w a s c a l c u l a t e d for e a c h site by averaging the p e r c e n t a g e of plots with at least o n e truffle collected during the  48 primary collection period.  Sampling of northern flying squirrels T o estimate the population s i z e of northern flying squirrels o n the five sites, live-trapping w a s c o n d u c t e d at approximately five- to s i x - w e e k intervals from M a y 1996 through  March  1999.  Trapping was  suspended when  snow  conditions  prevented vehicular a c c e s s to the sites or during e x c e s s i v e d i s t u r b a n c e by black b e a r s (Ursus americanus P a l l a s ) (e.g. late spring to early fall of 1998). Mark-recapture Sullivan  (1997)  and  methods  followed  R a n s o m e (2001).  p r o c e d u r e s reported One Tomahawk  by  R a n s o m e and  live-trap  (Model 201,  T o m a h a w k Live T r a p C o . , T o m a h a w k , W i s c o n s i n ) w a s m o u n t e d on a tree trunk (ca. 1.5 m a b o v e the ground) at e a c h of the 80 stations per grid. T h e traps w e r e e q u i p p e d with a container filled with c o a r s e brown cotton for nesting material, baited with a p i e c e of carrot a n d mixture of peanut butter a n d w h o l e oats, a n d c o v e r e d o n three s i d e s with a p i e c e of shingle roofing ( R a n s o m e a n d Sullivan 1997). T r a p s w e r e set in two c o n s e c u t i v e e v e n i n g s (one hour before dark) a n d c h e c k e d the following mornings. T r a p s w e r e l o c k e d o p e n during the trap d a y s a n d b e t w e e n s e s s i o n s .  A pre-bait of  sunflower s e e d s w a s a d d e d to the nest b o x e s b e t w e e n s e s s i o n s .  Both e a r s of  captured a n i m a l s w e r e  m a r k e d with individually n u m b e r e d e a r tags.  The  tag  n u m b e r s , location (station number), weight (± 5 g on a P e s o l a s c a l e ) , g e n d e r , a n d breeding condition ( K r e b s et al. 1969; M c C r a v y a n d R o s e 1992) w e r e recorded for captured a n i m a l s .  Estimating parameters of northern flying squirrel populations Mark-recapture data a n a l y s i s followed p r o c e d u r e s reported by R a n s o m e a n d  49 Sullivan (1997) a n d R a n s o m e (2001). E s t i m a t e s of population s i z e , trappability, a n d m o v e m e n t w e r e c a l c u l a t e d using the J o l l y - S e b e r m o d e l (Small Mammal for Mark-Recapture  Programs  Data Analysis, C . J . K r e b s , Department of Z o o l o g y , University of  British C o l u m b i a , V a n c o u v e r , B . C . V 6 T 2 A 9 ) modified for s m a l l s a m p l e s i z e s ( S e b e r 1982). S i n c e this m o d e l cannot estimate population s i z e s for the first a n d last trap s e s s i o n s , the m i n i m u m n u m b e r of a n i m a l s known to be alive ( M N A ; K r e b s 1966) w a s u s e d for t h e s e periods.  ' R e s i d e n t ' squirrels (captured at least twice) w e r e  included in e s t i m a t e s of population s i z e ; 'transient' squirrels (captured only o n c e ) w e r e r e m o v e d from the data prior to a n a l y s i s .  Trappability is the probability of a  m a r k e d a n i m a l in a population being included in the s a m p l e ( K r e b s a n d B o o n s t r a 1984).  T r a p s e s s i o n s w e r e g r o u p e d into three periods: winter ( S e p t e m b e r  -  February), spring ( M a r c h - M a y ) a n d s u m m e r (June - A u g u s t ) (following R a n s o m e 2001).  E s t i m a t e s of m e a n population s i z e a n d trappability w e r e calculated for e a c h  of t h e s e periods. During e a c h period, all sites had to be trapped at least o n c e with a trappability  exceeding  50%  to  be  included  in  further  analyses,  c o n s i d e r a t i o n s in Gilbert (1973) a n d K r e b s a n d B o o n s t r a (1984).  based  on  Movements were  calculated by a v e r a g i n g the d i s t a n c e s m o v e d by individuals b e t w e e n first-capture points on c o n s e c u t i v e trap s e s s i o n s .  Effective a r e a s a m p l e d w a s determined by  adding to the trapping grid a r e a a buffer of one-half of the m e a n d i s t a n c e m o v e d b e t w e e n s u b s e q u e n t recaptures.  Squirrel densities w e r e estimated by dividing the  population s i z e by the effective a r e a s a m p l e d .  Describing the diet of northern flying squirrels T o d e s c r i b e the diet of northern flying squirrels at the five study sites, f e c a l s a m p l e s w e r e obtained during live-trapping s e s s i o n s in 1997 a n d 1998 a n d w e r e  50 microscopically e x a m i n e d following histological p r o c e d u r e s modified from Mclntire a n d C a r e y (1989), C a s t e l l a n o et al. (1989), a n d C o l g a n (1997).  No fecal samples were  collected during the late spring to early fall of 1998; trapping w a s s u s p e n d e d at this time d u e to e x c e s s i v e disturbance by black b e a r s . F e c a l s a m p l e s w e r e collected only from individuals captured for the first time during e a c h live-trapping s e s s i o n to avoid inclusion of bait in the s a m p l e ( M a s e r et al. 1986).  Pellets (1 - 2 0 ) d e f e c a t e d during a n i m a l handling w e r e collected directly from  the a n u s into sterile vials to avoid contamination of the s a m p l e with s p o r e s or other materials from the environment ( C o l g a n 1 9 9 7 ; C a z a r e s et al. 1999).  Vials were  labeled with the location (grid, station), date, a n d individual squirrel tag n u m b e r s . F e c a l s a m p l e s w e r e initially p l a c e d in the freezer, a n d o n c e e n o u g h s a m p l e s h a d a c c u m u l a t e d , w e r e then p r e s e r v e d by drying in a dehydrator at 50°C for 2 4 hours. A l c o h o l ( 9 5 % ethanol) w a s later a d d e d to the s a m p l e s to prevent potential e x p o s u r e to Hantavirus ( C o l g a n 1997; R o s e n t r e t e r et al. 1997). In the laboratory, pellets w e r e c r u s h e d to a p o w d e r using a mortar a n d pestle, w e i g h e d to the nearest 0.01 g, a n d p l a c e d in a g l a s s vial.  U s i n g a micropipette,  b e t w e e n 0.1 to 1.0 m L of distilled water w a s a d d e d to the s a m p l e b a s e d on a dilution factor determined by the s a m p l e ' s dry weight (to e q u a l about four times the v o l u m e of dried material following C o l g a n et al. 1997). rehydrate  for  48  hours  at  room  T h e s a m p l e w a s left in the vial to  temperature  ( C a z a r e s et  al.  1999).  After  h o m o g e n i z i n g the s a m p l e thoroughly using a motorized pellet pestle, two d r o p s of the mixture w e r e p l a c e d on a c l e a n m i c r o s c o p e slide.  T w o d r o p s of M e l z e r ' s solution  ( C a s t e l l a n o et al. 1987) a n d 1 drop of lacto-glycerol w e r e a d d e d a n d the solution w a s stirred a n d c o v e r e d with a 2 2 x 4 0 m m coverslip. T h r e e s l i d e s w e r e prepared in this m a n n e r for e a c h f e c a l s a m p l e .  51 U s i n g a c o m p o u n d m i c r o s c o p e at 4 0 0 - x magnification, the p r e s e n c e of fungal s p o r e s , plant material a n d other items in the diet w a s recorded from 2 5 systematically located fields of view on e a c h slide. T h i s w a s converted to a percent o c c u r r e n c e of e a c h item out of the 7 5 p o s s i b l e fields of view e x a m i n e d per f e c a l s a m p l e (Rosentreter et al. 1997).  F u n g a l s p o r e s w e r e identified to the lowest p o s s i b l e t a x o n o m i c level,  using k e y s a n d descriptions in C a s t e l l a n o et al. (1989) a n d referring to p e r m a n e n t reference s l i d e s of h y p o g e o u s s p o r e s prepared from v o u c h e r s p e c i m e n s (from the M y c o l o g i c a l H e r b a r i u m at O r e g o n State University, Corvallis, O r e g o n ) . P l a n t material (including  vegetative  material  and  pollen)  was  identified  using  anatomical  characteristics including cell wall structure a n d the p r e s e n c e of v a s c u l a r e l e m e n t s , chloroplasts, t r i c h o m e s , starch g r a n u l e s , a n d s t o m a t a cells ( B a u m g a r t n e r a n d Martin 1939; J o h n s o n etal. 1983; W i k e e m a n d Pitt 1983). Other food items included insect parts  and  lichen  (identified from  the  p r e s e n c e of  algal cells; G o w a r d  1999).  Unidentifiable d i g e s t e d matter w a s o b s e r v e d in every s a m p l e , but not included in the analysis. S p o r e s a n d other m i s c e l l a n e o u s items that c o u l d not be positively identified a n d o c c u r r e d in trace a m o u n t s (less than 5 % of the fields of view; C o l g a n 1997) w e r e g r o u p e d into a n ' u n k n o w n ' category.  W h e r e n e e d e d , 100-x w a s u s e d to view larger  plant structures a n d 1000-x magnification w a s u s e d to further e x a m i n e fungal s p o r e s (see recommendations  in Mclntire a n d C a r e y 1989).  F e c a l s a m p l e s collected from resident squirrels w e r e  included in further  a n a l y s e s ; t h e s e a n i m a l s w e r e more likely than transient individuals to be eating from the study site. T o d e s c r i b e the s e a s o n a l diet of northern flying squirrels a n d facilitate c o m p a r i s o n s to other studies, data collected from the five sites during two y e a r s w e r e pooled by s e a s o n .  T w o m e t h o d s w e r e u s e d to d e s c r i b e the importance of v a r i o u s  items in the diet of northern flying squirrels: 1) the m e a n percent o c c u r r e n c e of e a c h  52 item in the diet w a s calculated for all f e c a l s a m p l e s collected within a s e a s o n or trapping s e s s i o n (termed  'relative a b u n d a n c e ' in C u r r a h et al. 2000) a n d 2) the  p e r c e n t a g e of f e c a l s a m p l e s containing a major food item within e a c h s e a s o n or trapping s e s s i o n w a s determined (termed 'frequency' in C u r r a h et al. 2000).  Foods  w e r e c o n s i d e r e d major if they had a m e a n relative a b u n d a n c e of at least 5 % of the fields of view within e a c h s e a s o n or trapping s e s s i o n (e.g. C o l g a n 1997). A l t h o u g h the o c c u r r e n c e of the s a m e truffle g e n e r a c a n be compared  a c r o s s s e a s o n s using  relative  a b u n d a n c e , caution  must  meaningfully be u s e d  if  c o m p a r i n g the relative a b u n d a n c e a m o n g truffle g e n e r a in f e c a l s a m p l e s collected within a s e a s o n .  T h i s a p p r o a c h is problematic, s i n c e different truffle taxa h a v e  different s i z e s a n d concentrations of s p o r e s ( C a s t e l l a n o et al. 1989). In addition, varied s p o r e s i z e s a n d d e g r e e of s p o r e ornamentation c a n affect gut p a s s a g e a n d retention  rates  (Mclntire  and  Carey  1989;  Pyare  and  Longland  2001a).  c o n s u m p t i o n of a n equivalent a m o u n t of truffle therefore m a y yield different  The spore  o c c u r r e n c e s in f e c a l s a m p l e s ( C a s t e l l a n o et al. 1989; C o l g a n 1997; T h y s e l l et al. 1997; P y a r e a n d L o n g l a n d 2 0 0 1 a ) .  Analyses T o a s s e s s the d e g r e e to which northern flying squirrels w e r e being selective in the fungi they c o n s u m e d a n d to determine w h i c h truffle taxa m a y be preferred, I c o m p a r e d truffle taxa e a t e n by resident squirrels to their a b u n d a n c e within a site a n d s e s s i o n . Truffle f r e q u e n c y (i.e. the p e r c e n t a g e of f e c a l s a m p l e s containing e a c h truffle taxa a s a major food item) w a s u s e d a s a m e a s u r e of overall importance in squirrel diets; standing crop (kg per ha) w a s u s e d a s a m e a s u r e of truffle a b u n d a n c e .  Fecal  s a m p l e s collected within a trapping s e s s i o n w e r e graphically c o m p a r e d to the most  proximal truffle s e s s i o n . intervals  in  53 S i n c e truffle s e s s i o n s o c c u r r e d at approximately ten-week  1998 a n d early  1999, a m a x i m u m  of five w e e k s s e p a r a t e d  group  c o m p a r i s o n s a n d trapping periods falling outside this period w e r e e x c l u d e d from analysis.  Determining if this time frame is appropriate biologically is difficult b e c a u s e  the p e r s i s t e n c e of truffle s p o r o c a r p s in the substrate a n d their fruiting period are not known for m a n y taxa ( F o g e l 1976; F o g e l a n d T r a p p e 1978). H o w e v e r , the major truffle s p e c i e s collected at the five sites are relatively long-lived a n d h a v e fruiting p e r i o d s that e x c e e d five w e e k s (e.g. Elaphomyces 1 9 8 1 ; Rhizopogon  granulatus a n d E. muricatus Fr., S m i t h et al.  vinicolor S m . , Smith a n d Z e l l e r 1966).  S e l e c t i v e b e h a v i o u r by  northern flying squirrels w a s a s s u m e d w h e n their u s e of truffle taxa ( a b u n d a n c e in diet) e x c e e d e d truffle availability ( a b u n d a n c e on site) ( J o h n s o n 1980), a s is the c a s e w h e n g e n e r a are over-represented in the diet relative to their a b u n d a n c e in the soil ( J o h n s o n 1994b).  M e a n n u m b e r s of truffle taxa c o n s u m e d by squirrels a n d found  during concurrent s a m p l i n g w e r e c o m p a r e d with a p a i r e d - s a m p l e t test (at a 0.05 level of significance). T h e P e a r s o n correlation coefficient (r) w a s c a l c u l a t e d to m e a s u r e the d e g r e e of a s s o c i a t i o n b e t w e e n the density of resident northern flying squirrels a n d the e s t i m a t e s of a n n u a l truffle production or m e a n percent f r e q u e n c y of plots with truffles o n e a c h site.  A strong positive relationship (significant at the 0.05 level) w a s a s s u m e d to be  consistent with the hypothesis that northern flying squirrels are food limited. D e n s i t i e s w e r e u s e d instead of e s t i m a t e s of population s i z e to correct for m o v e m e n t - r e l a t e d e d g e effects. S i n c e m e a s u r e s of a n i m a l density m a y not reflect differences in habitat quality, V a n H o m e (1983) r e c o m m e n d e d collecting survival a n d breeding information in addition to density.  H o w e v e r , no significant differences in m e a s u r e s of survival or  breeding w e r e detected in a larger related study at t h e s e sites ( R a n s o m e 2001), s o densities a l o n e w e r e u s e d .  54  RESULTS  Occurrence and abundance of truffle species at each site E l e v e n s p e c i e s from 6 g e n e r a w e r e identified from truffle collections during the primary collection period (April to D e c e m b e r 1998), including 7 a s c o m y c e t e s , 3 b a s i d i o m y c e t e s , a n d 1 z y g o m y c e t e (Table 9). N o additional g e n e r a b e y o n d t h o s e found during this period w e r e collected during the remaining s e s s i o n s in 1 9 9 7 or 1999 ( A p p e n d i x 1). A n u m b e r of Hydnotrya a n d Rhizopogon s p o r o c a r p s w e r e too immature for identification to s p e c i e s . S i x immature b a s i d i o m y c e t e s p o r o c a r p s a l s o could not b e identified to a lower t a x o n o m i c level. Elaphomyces truffle  w a s collected from the C h e h a l i s a n d R e s e a r c h Forest sites. U p to 10  species were  Elaphomyces  O n e u n d e s c r i b e d s p e c i e s of  found  at e a c h site  (Table  9) a n d s e s s i o n (Table 10).  granulatus w a s the only s p e c i e s collected in all s e s s i o n s at all five  sites ( T a b l e s 9 a n d 10). During the primary collection period, 1,923 truffles representing 1,704.06 g (dry weight) w e r e collected at the five sites (Table 11).  O n l y two s p e c i e s w e r e  c o n s i d e r e d major, i.e. c o m p r i s e d at least 5 % of the total n u m b e r or total b i o m a s s of truffles collected during this time (following Hering 1966). E . granulatus  contributed  8 7 % of the total n u m b e r a n d 9 1 % of the total b i o m a s s of truffles collected a n d E. muricatus contributed 6 % of the total n u m b e r a n d 8 % of the total b i o m a s s (Table 11). T h e remaining s p e c i e s represented 7 % of the total n u m b e r a n d l e s s than 1 % of the total b i o m a s s of truffles collected (Table 11). Thirty percent of the 1 0 7 6 plots s a m p l e d during the entire study a n d 2 7 % of the 6 2 6 plots s a m p l e d during the primary collection period h a d at least o n e truffle. During e a c h s e s s i o n , b e t w e e n 6 a n d 8 8 % of plots h a d at least o n e truffle (Table 12).  55 E. granulatus w a s found in 2 3 % a n d E. muricatus w a s found in 7 % of the 6 2 0 plots s a m p l e d during the primary collection period; the remaining s p e c i e s w e r e e a c h found in < 1% of the plots s a m p l e d during this time.  T a b l e 9.  Truffle s p e c i e s a n d type f o u n d at e a c h site during the primary collection period.  Site G e n u s and s p e c i e s  Type  CAP  CHEH  COQ  RF  SDF  A  X  X  X  X  X  Elaphomyces muricatus Fr.  A  X  X  X  X  Elaphomyces  A  Elaphomyces  granulatus Fr. sp.nov.  3  X  X  Endogone lactiflua Berk. & Br.  Z  X  Hydnotrya cubispora ( B e s s . & T h o m p s . ) Gilk.  A  X  Hydnotrya variiformis Gilk.  A  Hydnotrya  b  A  X  Picoa earthusiana Tul. & T u l .  A  X  Rhizopogon hawkerae S m .  B  X  sp.  Rhizopogon subclavitisporus  Sm.  B  Rhizopogon vinicolor S m .  B  Rhizopogon  B  sp  b  Tuber sphaerosporum Total s p e c i e s  Gilk.  A  X  X  X  X  X X X X 4  X  X  X 5  Total s e s s i o n s 4 4 A = Ascomycotina, B = Basidiomycotina, Z = Zygomycotina "truffles were too immature for identification to species.  4-5  8-10  3  4  4  4  56  T a b l e 10. Truffle s p e c i e s found at the five sites during e a c h s e s s i o n in the primary collection period.  Session (1998)  a  Genus and species Elaphomyces  granulatus  Summer  E. Fall  L. Fall  X  X  X  X  X  X  Elaphomyces  muricatus  X  X  Elaphomyces  sp. nov.  X  X  Endogone  lactiflua  Hydnotrya  cubispora  Hydnotrya  variiformis  X  Hydnotrya s p . Picoa  X  X  X  X  X  X  X  X  carthusiana  Rhizopogon Rhizopogon Rhizopogon  X  hawkerae  X  subclavitisporus  X  vinicolor  X  Rhizopogon s p .  X  Tuber  X  sphaerosporum  Total s p e c i e s  6-7  8-10  5-6  2  Total a r e a s a m p l e d (m ) 640 640 640 584 S p r i n g : 04/20 to 05/01; Summer: 06/29 to 07/17; Early Fall: 09/10 to 09/27; Late Fall: 11/21 to 12/19 2  a  Spring  57  T a b l e 1 1 . N u m b e r s a n d b i o m a s s (g dry weight) of truffle s p e c i e s found within 6 2 6 plots s a m p l e d during the primary collection period at the five sites.  Genus and species  No. of truffles  % of total Total % of total no. biomass (g) biomass  Elaphomyces  granulatus  1,670  86.8  1,555.20  91.26  Elaphomyces  muricatus  118  6.1  136.03  7.98  Elaphomyces  sp.nov.  4  0.2  0.94  0.06  1  0.1  0.05  0.00  Endogone  lactiflua  Hydnotrya  cubispora  15  0.8  0.47  0.02  Hydnotrya  variiformis  41  2.1  3.54  0.21  Hydnotrya sp.  20  1.0  0.59  0.03  Picoa  32  1.7  2.48  0.15  carthusiana  Rhizopogon  hawkerae  3  0.2  1.56  0.09  Rhizopogon  subclavitisporus  1  0.1  0.24  0.01  Rhizopogon  vinicolor  4  0.2  1.12  0.07  Rhizopogon sp.  4  0.2  0.20  0.01  Tuber  4  0.2  0.42  0.02  6  0.3  1.22  0.07  1,923  100  1,704.06  100  sphaerosporum  U n k n o w n immature truffles Totals  58 T a b l e 12. P e r c e n t a g e of plots with at least o n e truffle collected during e a c h s e s s i o n at the five sites both a) prior to a n d b) following c h a n g e s in the s a m p l i n g m e t h o d s . V a l u e s in p a r e n t h e s e s are the n u m b e r of 4 - m plots s a m p l e d per s e s s i o n . 2  Frequency of occurrence (%) in plots Time of sampling  CAP  CHEH  a) L S p r i n g  75.0 (24)  a) L S u m m e r  87.5 (24)  a) Fall  -  COQ  12.5 (24)  SDF  37.5 (24)  2 0 . 8 (24)  -  (0)  (0)  20.8(24)  2 9 . 2 (24)  -  (0)  9.4 (32)  12.5 (32)  2 5 . 0 (32)  (0)  16.0 (25)  31.0 (29)  -  (14)  RF  3  37.5 (32)  a) W i n t e r  53.1 (32)  b) Spring  65.6 (32)  18.8 (32)  28.1 (32)  12.5 (32)  18.8 (32)  b) S u m m e r  6 2 . 5 (32)  15.6 (32)  18.8 (32)  2 1 . 9 (32)  3 1 . 3 (32)  b) Early Fall  75.0 (32)  15.6 (32)  18.8 (32)  9.4 (32)  3 1 . 3 (32)  b) Late Fall  4 6 . 9 (32)  8.3 (24)  7.7 (26)  6.3 (32)  18.8 (32)  3 3 . 3 (24)  28.6 (28)  b) W i n t e r  --  -  -  (0)  (0)  -  (0)  -  (2)  M e a n ± SE 6 2 . 5 ± 5.8 14.6 ± 2 . 2 18.4 ± 4 . 2 12.5 ± 3 . 4 25.1 ± 3 . 6 percentages are not given for s e s s i o n s with less than 24 plots sampled, ^ a v e r a g e s are calculated for the four s e s s i o n s in the primary collection period (N = 4). S E = standard error of the m e a n b  E s t i m a t e s of the corrected standing crop of truffles for e a c h s a m p l i n g s e s s i o n ranged from 0.43 kg ha" at C h e h a l i s to 22.61 kg ha" at C a p i l a n o a n d from 4 4 9 1  1  truffles h a " at C o q u i t l a m to 2 6 , 2 6 4 truffles ha" at C a p i l a n o (Figure 2). T h e r e w e r e 1  1  no consistent s e a s o n a l patterns of truffle standing c r o p s (Figure 2).  T h e truffle  standing crop in C a p i l a n o far e x c e e d e d the other sites in all but o n e s e s s i o n (Figure  A n index of the a n n u a l production  of truffles for e a c h site w a s derived  following a n adjustment using site-specific correction factors (Tables 13 a n d 14). T h i s index ranged from 1.68 kg h a " in the R e s e a r c h F o r e s t to 15.72 kg h a " 1  1  in  C a p i l a n o a n d from 2,228 truffles ha" in C o q u i t l a m to 2 0 , 4 4 9 truffles ha" in C a p i l a n o 1  (Table 14).  1  59  25.00  CAP  CHEH  -€^-COQ  - X - R F  SDF  co 20.00 A CD  co 15.00 H o  £ g>  10.00 5.00 -X  0.00 Spring  Summer Season  -A-CAP  Spring  CHEH  Summer Season  E Fall  (1998,  early  L Fall  1999)  -€>-COQ  - X - R F  E Fall  L Fall  (1998,  early  Winter  SDF  Winter  1999)  Figure 2. T h e corrected standing crop of truffles collected on e a c h site during the primary collection period a n d early 1999, s t a n d a r d i z e d to b i o m a s s per hectare (A) a n d n u m b e r per hectare (B). S a m p l i n g effort w a s consistent for the first four s e s s i o n s ; only two sites w e r e s a m p l e d in winter 1999.  60  T a b l e 13. S u m m a r y of the v a l u e s from the habitat s u r v e y u s e d to determine correction factors for standardizing truffle production on a per hectare basis.  Proportion of transect occupied by objects Mean (%) (N = 10)  SE  Correction Factor  CAP  18.01  0.75  0.8199  CHEH  16.73  1.71  0.8327  COQ  17.95  0.66  0.8205  RF  14.27  0.51  0.8573  1.33  0.8795  Site  SDF 12.05 S E = the standard error of the m e a n .  T a b l e 14. Indices of truffle production for e a c h site b a s e d on standing c r o p s from the primary collection period.  Weight (kg) ha" year" 1  1  Number ha" year" 1  1  Site  Estimate (SE)  Corrected" (SE)  Estimate (SE)  Corrected" (SE)  CAP  19.17 (3.22)  15.72 (2.64)  2 0 , 4 4 9 (4,366)  16,766 (3,589)  CHEH  2.20 (0.70)  1.83 (0.59)  3,151 (637)  2,624 (531)  COQ  2.90 (0.73)  2.38 (0.60)  2 , 7 1 5 (865)  2,228 (710)  RF  1.96 (0.54)  1.68 (0.46)  3,418 (527)  2,930 (452)  3  3  SDF 7.29 (2.30) 6.41 (2.02) 7,930 (2,547) 6,974 (2,240) C a l c u l a t e d by averaging the truffle standing crops (biomass or numbers per hectare) for the four sessions in the primary collection period (equivalent to 'method 2' in Hunt and Trappe 1987). a correction factor to account for differences in amount of bare ground area between sites w a s applied. S E = the standard error of the m e a n b  61  Importance of truffles in the year-round diet of northern flying squirrels I m i c r o s c o p i c a l l y e x a m i n e d 195 f e c a l s a m p l e s from 125 individual northern flying squirrels captured at the five sites over two y e a r s (Table 15). F e c a l s a m p l e s w e r e collected from 5 4 % of the squirrels live-trapped for the first time during e a c h trapping period. A total of 176 f e c a l s a m p l e s w e r e collected from resident squirrels a n d w e r e included in further a n a l y s e s (Table 15).  T a b l e 15. N u m b e r of f e c a l s a m p l e s e x a m i n e d within e a c h s e a s o n collected from northern flying squirrels during two y e a r s of live-trapping at five sites.  No. of fecal samples examined R T  No. of individual squirrels R T  21  1  19  1  36  7  34  7  S u m m e r 1997  12  1  12  1  Fall 1997  14  2  14  2  W i n t e r 1998  66  4  48  4  S p r i n g 1998  11  2  11  2  S u m m e r 1998  ~  —  ~  —  Fall 1998  16  2  16  2  Season W i n t e r 1997 Spring 1997  Total 'determined from individuals.  t  9  176 19 106 19 individually n u m b e r e d e a r tags; R = resident, T = transient  Plant material w a s c o n s u m e d year-round by northern flying squirrels a n d o c c u r r e d a s a major food item in all s a m p l e s e x a m i n e d (Figure 3).  F u n g i (as  determined by the p r e s e n c e of fungal s p o r e s ) w a s a major food item in 6 6 % of the f e c a l s a m p l e s collected y e a r - r o u n d . T h e proportion of total s a m p l e s containing fungi a s a major food varied s e a s o n a l l y , ranging from 5 7 % of s a m p l e s in spring to 1 0 0 % of s a m p l e s in s u m m e r (Figure 3).  A l t h o u g h both e p i g e o u s a n d h y p o g e o u s fungal  62 taxa w e r e identified a n d included in the 'fungal s p o r e ' group, l e s s than 1% of the s a m p l e s contained only e p i g e o u s s p o r e s a s a dominant f o o d . O t h e r identifiable food items, s u c h a s insect parts a n d lichens, mostly o c c u r r e d in trace a m o u n t s w h e n present; l e s s than 3 % of the total s a m p l e s e x a m i n e d c o n t a i n e d 'other' items a s a major food p e r s e a s o n (Figure 3).  Winter (87)  Spring (47)  Summer (12)  Fall (30)  Figure 3. T h e p e r c e n t a g e of f e c a l s a m p l e s within e a c h s e a s o n that c o n t a i n e d 'major' food items (i.e. o c c u r r e d in at least 5 % of the 7 5 fields e x a m i n e d per s a m p l e ) . T h e n u m b e r of f e c a l s a m p l e s e x a m i n e d during e a c h s e a s o n is given in p a r e n t h e s e s .  The frequency  ( F R ) a n d relative  abundance  ( R A ) of major  foods  that  r e m a i n e d detectable in f e c a l s a m p l e s a r e p r e s e n t e d by s e a s o n in T a b l e 16. Plant material,  including  undigested  vegetative  elements, w a s a common component  t i s s u e s , pollen  grains, a n d v a s c u l a r  of the diet of northern  flying  squirrels,  e s p e c i a l l y in the winter, spring a n d fall ( 1 0 0 % F R , > 7 1 % R A , T a b l e 16). P o l l e n grains, most c o m m o n l y from alder (Alnus spp.), o c c u r r e d in large quantities within fecal s a m p l e s collected from M a r c h to M a y of both y e a r s , s u g g e s t i n g ingestion of  63 staminate c o n e s of both coniferous a n d d e c i d u o u s s p e c i e s ( M a s e r et al. 1985). Eight truffle g e n e r a (or morphologically similar groups) w e r e classified a s major food items within e a c h s e a s o n (Table 16). Elaphomyces  w a s the only truffle  g e n e r a ingested year-round by northern flying squirrels a n d w a s a major f o o d in 5 0 % of the 176 s a m p l e s e x a m i n e d .  Melanogaster  a n d Rhizopogon  w e r e present a s a  major food in three s e a s o n s ; the remaining truffles w e r e c o n s u m e d a s a major food during o n e or two s e a s o n s . Truffle ingestion p e a k e d in the s u m m e r a n d fall with the most d i v e r s e array of fungal taxa occurring in squirrel diets in s u m m e r .  Rhizopogon  w a s a major food in the spring, s u m m e r a n d fall diets; c o n s u m p t i o n p e a k e d in the fall (Table 16). S e v e r a l additional truffle g e n e r a o c c u r r e d in s e c o n d a r y ( 1 - 5 % R A ) or trace (< 1%  RA) amounts  Leucophleps,  per  season,  including:  Chamonixia,  Endogone,  Hydnotrya,  Octavianina, Picoa, a n d Tuber. T h e significance of t h e s e o c c u r r e n c e s  in the diet of squirrels is difficult to interpret; they could represent food  items  c o n s u m e d in s m a l l quantities at the time of s a m p l i n g , or be remnant s p o r e s from a previous m e a l . T h e n u m b e r of truffle taxa that I found during truffle s e s s i o n s a n d o b s e r v e d in the diets of northern flying squirrels is p r e s e n t e d over time for e a c h site in A p p e n d i x 2 a n d s u m m a r i z e d in T a b l e 17. Northern flying squirrels c o n s u m e d nine truffle taxa that w e r e not collected during fungal s u r v e y s (Table 17). B a s e d on the p r e s e n c e of truffle s p o r e s in f e c a l s a m p l e s , b e t w e e n 1 to 8 additional truffle taxa m a y be present on e a c h site (Table 17). T h e n u m b e r of taxa found by mycologists a n d squirrels at e a c h site represents a ' m i n i m u m ' number; any rare truffle taxa that m a y h a v e b e e n present on the site but not found during truffle s a m p l i n g a n d not c o n s u m e d by squirrels would not be included in this table.  A critical a s s u m p t i o n is that resident  T a b l e 16.  M a j o r food i t e m s " by s e a s o n that were observed in fecal s a m p l e s collected from resident northern flying squirrels at the five sites b e t w e e n J a n u a r y 1997 and D e c e m b e r 1998.  Winter (N = 87) Food Item  FR (%)  Plant Material  Spring (N = 47) FR  a  Summer (N = 12) FR  a  Fall (N = 30) FR  a  (%)  RA" (SE)  (%)  100  9 5 . 4 (0.9)  100  86.6 (3.5)  100  57  21.1 (3.6)  43  9.8 (3.1)  33  FR  a  a  (%)  RA" (SE)  (%)  RA" (SE)  51.9 (6.3)  100  71.0 (5.3)  100  86.0(1.7)  23.4(11.3)  48  19.4 (6.1)  50  RA" (SE)  RA" (SE)  Overall (N = 176)  H y p o g e o u s Fungi A) Ascomycotina  Elaphomyces  —  —  21  9.3 (3.6)  Rhizopogon  —  —  11  9.0 (4.1)  Thaxterogaster  —  —  —  5.6 (2.3)  Genea  —  ~  ~  ~  ~  18.1 (2.4)  --  B) Basidiomycotina 0  Melanogaster  17  72  17.2 (2.7)  —  17  16.7 (11.2)  —  —  50  35.3(13.6)  31  15.5(6.4)  19  67  41.7 (13.0)  24  11.7 (5.6)  ~  —  —  —  —  —  —  —  —  —  —  Hysterangium  —  ~  —  ~  8  8.1 (8.1)  —  —  ~  —  8  8.3 (8.3)  —  Leucogaster  24  54.1 (14.0)  Russulaceae ' 0  55.3 (8.8)  58  —  —  —  — 7.8(1.9)  — ~ 38 12.7 (5.0) 8.2 (8.2) 8 -— — — Epigeous Fungi F R (Frequency) is the percentage of fecal samples containing a given food item within each season; R A (Relative Abundance) is the mean percent frequency of occurrence of a dietary item (out of 75 possible fields of view per sample) for all fecal samples collected within each season {following Currah et al. 2000). Major seasonal food items have a mean relative abundance of at least 5% within each season; Rhizopogon: may include taxa that cannot be distinguished from Rhizopogon on the basis of spore morphology (Castellano et al. 1989); ''hypogeous genera of the Russulaceae family can only be reliably distinguished using both spore and sporocarp morphology (Castellano etal. 1989).  a  b  c  64  65 T a b l e 17. T h e n u m b e r of truffle taxa found during truffle s e s s i o n s (S) a n d in the diet (D) of northern flying squirrels.  Truffle genera by site CAP Taxa  S  Chamonixia  D  CHEH S  D  COQ S  D  RF S  SDF D  S  X  Elaphomyces  X  X  Endogone  X  Genea  X  Hydnotrya  X X  X  X  X  X  X  X  X X X  Hysterangium  D  X  X X  Leucogaster  X  X X  X  X  X X  X  X  X  X  X  Leucophleps  X  X  X  X  X  Melanogaster  X  X  X  X  X  Octavianina  X  X  Picoa Rhizopogon  (group)  X  X  Russulaceae  X  Thaxterogaster  X  Tuber N u m b e r of s a m p l e s  X  X  X  X  X 3  7  18  6  X X  X  X  X  X  X  X  X  36  9  45  8  X  X  X X  20  6  57  N u m b e r of t a x a 3 11 4 12 3 10 5 6 2 9 M i n i m u m n u m b e r of taxa 12 12 10 8 9 n u m b e r of s a m p l e s : S = the n u m b e r of c o m p l e t e (> 24 plots) truffle s e s s i o n s c o n d u c t e d at e a c h site; D = the n u m b e r of f e c a l s a m p l e s e x a m i n e d from resident northern flying squirrels at e a c h site. ^minimum n u m b e r of taxa present at e a c h site, b a s e d on both truffle collections a n d the p r e s e n c e of fungal s p o r e s in the diets of northern flying squirrels. 6  a  66 squirrels trapped o n the live-trapping grid are either foraging on the site or in adjacent similar habitat c h a r a c t e r i z e d by similar truffle c o m m u n i t i e s .  Selection of truffle taxa by northern flying squirrels Twenty site-diet pairings from 1997 through 1998 fell within a 5-week period (Figures 4 to 8) a n d w e r e u s e d to c o m p a r e taxa in squirrel diets to t h o s e on the site during concurrent s a m p l i n g . Northern flying squirrels c o n s u m e d significantly m o r e (f = 3 . 5 1 , df = 19, p = 0.002) truffle t a x a than w e found during concurrent truffle s a m p l i n g ; a n a v e r a g e of 2.8 ( S E = 0.41) truffle taxa w e r e o b s e r v e d a s a major food in f e c a l s a m p l e s a n d 1.5 ( S E = 0.14) truffle taxa w e r e found on the site. T h i s pattern r e m a i n e d consistent within this five-week  period; e v e n during the s a m e w e e k ,  northern flying squirrels c o n s u m e d on a v e r a g e 1.7 times m o r e (t = 2.80, df = 8, p = 0.023) truffle t a x a than w e collected in the field. Elaphomyces  (ELAP)  was  under-represented  in the  diet  relative  to  its  a b u n d a n c e in the field, e s p e c i a l l y w h e n c o m p a r e d to the f r e q u e n c y of other truffle g e n e r a found in f e c a l s a m p l e s . A l t h o u g h this g e n u s w a s c o m m o n both in the diet of squirrels a n d on the five sites (e.g. F i g u r e s 4, 5 A , 5 B , 5 D , 6, 7 C , 7 D , a n d 8), s o m e notable e x c e p t i o n s e m e r g e d .  Elaphomyces  s p o r e s w e r e not a major food item in  f e c a l s a m p l e s collected in the spring of 1997 at the R e s e a r c h F o r e s t (Figure 7 A ) , the s u m m e r of 1997 at C h e h a l i s (Figures 5 C ) , a n d the late fall of 1997 at the R e s e a r c h Forest (Figures 7 B , 7 E ) , e v e n though concurrent s a m p l i n g revealed standing c r o p s of Elaphomyces  significant  at the sites. Other truffle g e n e r a o c c u r r e d a s major  food items with similar (e.g. F i g u r e s 6 B ) or higher (e.g. Figure 5 B - D , 7 C , 7 E , 8 B ) f r e q u e n c y p e r c e n t a g e s than Elaphomyces, rare on the site.  e v e n though they w e r e u n c o m m o n to  67 Hydnotrya  ( H Y D N ) a l s o w a s u n d e r - r e p r e s e n t e d in northern flying squirrel  diets relative to its a b u n d a n c e on the sites.  F o r e x a m p l e , although s m a l l standing  c r o p s of Hydnotrya w e r e found in C a p i l a n o (Figures 4 A , 4 B ) , C h e h a l i s (Figure 5 A , 5 B , 5 C ) , C o q u i t l a m (Figure 6 A ) , a n d the R e s e a r c h Forest (Figure 7 B ) , s p o r e s of this g e n e r a w e r e not detected in the diet of squirrels during concurrent s a m p l i n g . A n u m b e r of truffle taxa present in squirrel diets w e r e not found on the site (i.e. u n c o m m o n to rare) during concurrent truffle s a m p l i n g : Rhizopogon Russulaceae  (RUSS),  (ENDO),  Octavianina  ( O C T A ) , Chamonixia ( C H A M ) , Thaxterogaster ( T H A X ) , Genea ( G E N E ) ,  Leucogaster  ( L E U G ) , Leucophleps  Hysterangium  (HYST),  Endogone  (RHIZ),  ( L E U P ) , Tuber ( T U B E ) , a n d Melanogaster  (MELA).  While  t h e s e taxa a l s o w e r e not usually c o m m o n in the diet, s o m e of the g e n e r a o c c u r r e d a s a major food item in the majority of f e c a l s a m p l e s e x a m i n e d (Figures 4 to 8).  Relationship between densities of resident northern flying squirrels and truffle production A total of 130 resident northern flying squirrels w e r e captured 5 8 6 times during  live trapping  o n the five study a r e a s from  M a y 1996 to M a r c h 1999.  E s t i m a t e s of the population s i z e of resident flying squirrels live-trapped at e a c h site ranged from 2 to 31 squirrels (Figure 9).  M e a n a b u n d a n c e of northern  flying  squirrels for e a c h period ranged from 3 squirrels in C a p i l a n o to 2 9 squirrels in the S e y m o u r Demonstration F o r e s t (Table 18). M e a n e s t i m a t e s of trappability for e a c h period ranged from 1 6 . 7 % in the R e s e a r c h F o r e s t to 1 0 0 % in C a p i l a n o (Table 19). T w o periods, winter 1997/98 a n d spring 1998, had at least o n e trap visit at e a c h site with trappability e s t i m a t e s e x c e e d i n g 5 0 % (Table 19) a n d w e r e included in further a n a l y s e s (Table 20). M e a n squirrel m o v e m e n t s on first c a p t u r e s of c o n s e c u t i v e trap  • Site (May 1997)  Diet (Apr. 1997) A  100  50.0  80  40.0  HSite (Feb. 1998)  - D i e t (Feb. 1998)  CD -C  c o  CO CL O  L— o  C/J  c o o  CO  c c  CD  TJ  Site (May 1997)  CD CD it  - Diet (Jul. 1997) 100  0  -  N ^  2 I  :  W  h  -  O  T  I  L  O U  <  2 O  > O  <  L  I  -  U O  Q -  B Site (Apr. 1998)  - Diet (Mar. 1998)  100  . I  LU  ^ O  X (_)  X H  LU CD  LU — 1  Truffle genera  Figure 4 .  T h e s t a n d i n g crop of truffle taxa found at C a p i l a n o and the frequency of truffle taxa in the diet (i.e % of fecal s a m p l e s containing e a c h truffle taxa a s a major food item) during concurrent (within 5 w e e k s ) s a m p l i n q N u m b e r of f e c a l s a m p l e s e x a m i n e d : N = 3 (D), N = 5 (A, B, C ) . 68  Zl  r  o  4.0  a Site (Jun. 1997)  - Diet (May 1997)  H S i t e (Jun. 1997)  Diet (Jun. 1997)  4.0  • Site (Jun. 1997)  - Diet (Jul. 1997)  • Site (Nov. 1997)  - Diet (Nov. 1997)  100  3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0  Truffle genera  Figure 5.  Truffle genera  T h e standing c r o p of truffle t a x a found at C h e h a l i s and the frequency of truffle taxa in the diet (i.e. % of fecal s a m p l e s containing e a c h truffle taxa a s a major food item) during concurrent (within 5 w e e k s ) s a m p l i n g . N u m b e r of f e c a l s a m p l e s e x a m i n e d : N = 3 (C), N = 4 (B), N = 5 (A, D). 69  • Site (Jun. 1997)  - Diet (May 1997)  16.0 -  100  100  Ei Site (Feb. 1998)  - Diet (Mar. 1998)  II Site (Sept. 1998)  - Diet (Oct. 1998)  B  14.0 -  100  100  12.0 10.0 8.0 -- 40  6.0 4.0 2.0 -  "  •  0.0 CL HI  20  —  '}„  1 Q > I  1 111  m  1 N  1 ^  ZD  1 CO CO ZD  1 111 Z 111  0 Q_ ZD HI  DU Truffle genera  Figure 6.  Truffle genera  T h e standing crop of truffle t a x a found at Coquitlam and the frequency of truffle taxa in the diet (i.e. % of f e c a l s a m p l e s containing e a c h truffle taxa a s a major food item) during concurrent (within 5 w e e k s ) sampling. N u m b e r of f e c a l s a m p l e s e x a m i n e d : N = 4 (A), N = 5 (C), N = 7 (D), N = 9 (B).  70  B S i t e (Jun. 1997)  co  m Site (Dec. 1997)  - Diet (Jun. 1997)  - Diet (Dec. 1997)  O S i t e (Feb. 1998)  100  - Diet (Jan. 1998)  100  80  80  60  60  40  40  20  20  0  0 • Site (Feb. 1998)  100  - Diet (Feb. 1998)  100  c o  80  E  60  c o o  CL  80  CO  CD  40 20 0 • Site (Dec. 1998)  - Diet (Nov. 1998) 100  Truffle genera  80  Figure 7. T h e standing crop of truffle taxa found at the R e s e a r c h Forest and the frequency of truffle taxa in the diet (i.e. % of fecal samples containing each truffle genera a s a major food item) during concurrent (within 5 weeks) sampling. Number of fecal s a m p l e s examined: N = 1 (A, E), N = 3 (D), N = 5 (B, C ) .  60 40 20 0  71  Truffle genera  o 'ST  H Site (Nov. 1997)  - Diet (Nov. 1997) B  100 80  HSite  --  CO  60  CJ)  —  _  'V''': ^ ffs'l  CL  O i—  o  --  -- 40 --  CJ)  c  1  20  m Site (Nov. 1998)  a. E CO  1  0  03  to  c o  - Diet (Nov. 1998)  CD 3  -  c o o CD  100 80  3  O 'co  -- 60 Truffle genera 40 + 20 0  Q_ UJ  I  CO  co a:  Truffle genera  F i g u r e 8.  T h e standing crop of truffle t a x a found at the S e y m o u r Demonstration Forest and the frequency of truffle taxa in the diet (i.e. % of f e c a l s a m p l e s containing e a c h truffle taxa a s a major food item) during concurrent (within 5 w e e k s ) s a m p l i n g . N u m b e r of f e c a l s a m p l e s e x a m i n e d : N = 6 (B, C ) , N = 13 (A).  72  73 s e s s i o n s for t h e s e periods ranged from 37 m in the R e s e a r c h F o r e s t to 99 m in the S e y m o u r D e m o n s t r a t i o n F o r e s t (Table 20).  B a s e d o n t h e s e m o v e m e n t s , the  effective trapping a r e a of the sites ranged from 12.6 h a in the R e s e a r c h F o r e s t to 17.5 h a in the S e y m o u r Demonstration Forest (Table 20). ranged from 0.56 squirrels h a  - 1  M e a n squirrel density  in C a p i l a n o to 1.21 squirrels h a " in the S e y m o u r 1  Demonstration Forest (Table 20). A significant positive correlation b e t w e e n densities of squirrels a n d truffles at the five study a r e a s would be consistent with the hypothesis that truffle r e s o u r c e s on a site limit the n u m b e r of resident squirrels. H o w e v e r , correlation  coefficients  describing the intensity of a s s o c i a t i o n b e t w e e n squirrel densities a n d indices of a n n u a l truffle production at the five sites did not support this hypothesis (index of production, r = - 0 . 2 1 , df = 3, p > 0.50; percent f r e q u e n c y in plots, r = - 0 . 3 0 , df = 3, p > 0.50; Figure 10).  E x c l u d i n g C a p i l a n o from the a n a l y s e s dramatically improved the  d e g r e e of a s s o c i a t i o n ; without C a p i l a n o the density of flying squirrels on a site w a s significantly correlated with indices of a n n u a l truffle production (r = 0.96, df = 2, p < 0.05) a n d truffle percent f r e q u e n c y in plots (r = 0.99, df = 2, p < 0.01) at a 0.05 level of significance (Figure 10).  Estimated population size —ro cn o  May-96 ~ > Aug-96 J Nov-96  x  Feb-97 May-97 ; Aug-97 ~_ Nov-97  x  o  Feb-98 May-98 Aug-98 ~\ 0  Nov-98 o  Feb-99 0  ro cn  co o  co cn  T a b l e 18.  M e a n e s t i m a t e d population s i z e from mark-recapture of northern flying squirrels during e a c h s e a s o n in o v e r two y e a r s of live trapping.  Mean estimated population size (SE)  5  Site  Winter 1996/97  CAP CHEH COQ RF SDF  N  Spring 1997  N  6.0(2.1)  3  13.7(1.7)  2  10.7(0.5)  3  20.9(0.5)  -  -  3.5(0.5)  2  Summer 1997  N  Winter 1997/98  Spring 1998  N  12.8 (--)  1  9.6(2.7)  2  5.7 (--)  1  3.0 (--)  1  --  -  2  21.9(9.1)  2  11.7(0.3)  2  11.0 (-)  1  5.0 (-)  1  --  --  22.3(1.7)  3  18.2 (--)  1  13.3 (--)  1  10.6 (--)  1  10.5(0.6)  2  7.0 (--)  1  7.3(1.3)  3  6.0 (--)  1  7.1 (0.9)  2  9.5 (--)  1  3  2.0 (-)  1  2  9.0(0.0)  2  N  19.5(3.8) 4 29.3(1.0) 2 2 9 . 4 (-) 1 20.2(0.5) 2 22.1 (0.9) 2 N = n u m b e r of e s t i m a t e s of population s i z e in the s a m p l e . W i n t e r = S e p t e m b e r to F e b r u a r y ; S p r i n g = M a r c h to M a y ; S u m m e r = J u n e to A u g u s t S E = s t a n d a r d error of the m e a n  75  Winter 1998/99  4.1 (0.7) 13.8(1.5)  N  Spring 1999  N  T a b l e 19.  M e a n e s t i m a t e d Jolly trappability of northern flying squirrels live-trapped at five sites during e a c h s e a s o n .  Mean estimated trappability (SE)  £  Site  Winter 1996/97  N  Spring 1997  N  Summer 1997  CAP  100.0(0.0)  3  58.0(33.0)  2  7 0 . 6 (-)  64.8(6.3)  3  76.4(2.9)  2  27.0(4.4)  2  89.6(10.4)  -  74.0 (4.9)  3  55.0 (--)  1  1  25.5(7.8)  3  16.7 (--)  1  N  1  69.7(11.5)  2  Spring 1998  N  Winter 1998/99  N  70.6 (-)  1  --  -  2  6 3 . 6 (-)  1  --  -  90.1 (--)  1  7 5 . 7 (-)  1  71.6(1.0)  2  84.1 (3.4)  2  6 3 . 2 (-)  1  92.1 (7.9)  3  ( -9) ^ 87.4(4.8) 2 5 1 . 0 (-) 1 69.1 (13.1) 2 7 7 . 4 ( 1 2 . 2 ) 2 N = n u m b e r of estimates of trappability in the s a m p l e . W i n t e r = S e p t e m b e r to F e b r u a r y ; S p r i n g = M a r c h to M a y ; S u m m e r = J u n e to A u g u s t S E = s t a n d a r d error of the m e a n  90.5(1.3)  2  CHEH COQ  --  RF -SDF  N  Winter 1997/98  7 5 . 0 (-)  9  3  2  3  76  Spring 1999  N  5 5 . 6 (-)  1  77  Table 20.  M e a n squirrel m o v e m e n t , effective trapping a r e a , a n d e s t i m a t e s of squirrel density.  Density (number ha" ) Mean Winter Spring density 1997/98 1998 (N=2) (SE) 1  Mean movement (m) (SE)  N  Effective trapping area (ha)  CAP  52.4 (17.1)  8  13.7  0.70  0.42  0.56 (0.14)  CHEH  89.7 (26.2)  17  16.6  0.70  0.66  0.68 (0.02)  COQ  56.8 (7.2)  15  14.0  0.95  0.76  0.85 (0.10)  RF  37.4 (14.2)  9  12.6  0.56  0.75  0.66 (0.10)  99.8 (9.6) 42 17.5 S E = s t a n d a r d error of the m e a n  1.15  1.26  1.21 (0.05)  SDF  78  2.0 1.8 CD 1.6 E 1.4 C 1.2 1.0 CO C 0.8 CD "O 0.6 0.4 0.2 CO 0.0  A CAP OCHEH  OCOQ  X RF  BSDF r = -0.21 a  r*=  -  0.96  •  -  A  0.0  5.0  10.0  15.0  20.0  Index of annual truffle production (kg ha" year" ) 1  ~2.0 2 1.8 a3 1.6 E 1.4 |1.2 % 1.0 'g 0.8 % 0.6 2: 0.4 3 0.2 CO 0.0  A CAP OCHEH  <§>COQ  X RF  •  1  SDF  r = -0.30 a  = 0.99  • xo  A  20  40  60  80  Mean frequency of plots with truffles (%)  Figure 10. T h e relationship b e t w e e n the a b u n d a n c e a n d o c c u r r e n c e of truffles a n d the densities of northern flying squirrels at e a c h site. Correlation coefficients are p r e s e n t e d on e a c h graph for two s c e n a r i o s : including C A P (r ) a n d excluding C A P (r ). a  6  79  DISCUSSSION  Truffles w e r e found in 3 0 % of the plots s a m p l e d in this study a n d 2 7 % of the plots s a m p l e d during  the primary  collection period.  This sampling  efficiency  e x c e e d e d ( 1 5 % , C o l g a n et al. 1 9 9 9 ; 2 3 % , North et al. 1997) or e q u a l e d ( 2 9 % , W a t e r s et al. 1994; 3 0 % W a t e r s ef al. 1997) the overall f r e q u e n c y reported by other r e s e a r c h e r s using similar s a m p l i n g t e c h n i q u e s (e.g. 4 - m circular plots) in the P a c i f i c 2  Northwest.  F r e q u e n c y of truffle o c c u r r e n c e in plots s h o u l d b e c o m p a r e d a m o n g  studies with caution b e c a u s e t h e s e v a l u e s a r e affected by differences in s a m p l i n g m e t h o d s , s u c h a s the s i z e a n d n u m b e r of plots a n d the time of s a m p l i n g (e.g. c o n d u c t e d during frequency  'peak' fruiting periods v e r s u s less productive times).  v a l u e s a l s o reflect  differences  in truffle c o m m u n i t i e s  Overall  among  sites,  including s p e c i e s c o m p o s i t i o n a n d s p e c i e s - s p e c i f i c fruiting patterns (e.g. c l u m p e d v e r s u s d i s p e r s e d , c o m m o n v e r s u s rare, long-lasting v e r s u s e p h e m e r a l ) a n d site factors (e.g. macroclimatic a n d microhabitat features) that affect truffle fruiting. Truffle collections w e r e d o m i n a t e d by o n e s p e c i e s , Elaphomyces  granulatus,  w h i c h represented 9 1 % of the total standing crop (dry weight) of truffles collected at the five study sites. A similar result w a s found in the only other published study that s a m p l e d truffle c o m m u n i t i e s in w e s t e r n h e m l o c k forests of the Pacific Northwest (Table 3, North et al. 1997).  E. granulatus a l s o d o m i n a t e d their truffle collections,  comprising 9 2 . 8 % of the total standing crop from three forest types c h a r a c t e r i z e d by different disturbance regimes a n d stand a g e s (North ef al. 1997). In a mature ( 1 8 0 year-old) Pacific silver fir s t a n d in W a s h i n g t o n , E. granulatus c o m p r i s e d the entire standing crop of h y p o g e o u s s p e c i e s collected during a six-month s a m p l i n g period (Vogt etal. 1981).  80 A l t h o u g h E. granulatus  has been described a s widespread and common  (Smith et al. 1981), it is l e s s predominant in other studies in the P a c i f i c Northwest. F o r e x a m p l e , in s t a n d s d o m i n a t e d by Douglas-fir, E. granulatus represented at most 2 7 % of the total standing crop ( L u o m a et al. 1991); m o r e often this s p e c i e s w a s either  not found  (e.g. Hunt  and Trappe  1 9 8 7 ; C l a r k s o n a n d Mills  1994) or  represented a minor c o m p o n e n t of truffle collections (i.e. < 5 % of the total b i o m a s s , F o g e l 1976; C a z a r e s et al. 1999; C o l g a n et al. 1999). did not collect Elaphomyces  Similarly, W a t e r s et al. (1994)  in m a n a g e d red fir a n d white fir forests of California.  A l t h o u g h W a t e r s et al. (1997) found three Elaphomyces  s p e c i e s in old-growth a n d  mature fir s t a n d s , they all represented minor contributions to truffle collections. W h y did E . granulatus dominate truffle collections in this s t u d y ?  C l u s t e r s of  E. granulatus s p o r o c a r p s h a v e b e e n positively a s s o c i a t e d with substrates containing high densities of fine roots a n d thick, matted organic layers (North et al. 1997; North a n d G r e e n b e r g 1998). S u c h conditions w e r e present to s o m e d e g r e e at all sites, but w e r e e s p e c i a l l y characteristic of C a p i l a n o , w h e r e s h a l l o w rooting tree s p e c i e s (e.g. western h e m l o c k a n d P a c i f i c silver fir) d o m i n a t e d a n d a m o r h u m u s layer up to 3 0 c m d e e p o c c u r r e d within truffle plots.  S u c h substrates m a y a c c o u n t for the high  f r e q u e n c y a n d b i o m a s s v a l u e s of E . granulatus found at this site.  In addition to a  t e n d e n c y to fruit prolifically in clusters under favourable conditions (Smith et al. 1981), E. granulatus a l s o p r o d u c e s heavy (Hunt a n d T r a p p e 1987) a n d long-lived (Hunt a n d T r a p p e 1 9 8 7 ; L u o m a et al. 1 9 9 1 ; J o h n s o n 1994a) s p o r o c a r p s c o m p a r e d to other truffle s p e c i e s , which c a n lead to high standing crop estimates (Hunt a n d T r a p p e 1987; L u o m a et al. 1 9 9 1 ; V o g t et al. 1992). A l t h o u g h standing c r o p s at s o m e sites in this study (e.g. S e y m o u r Demonstration extreme  compared  to  those  reported  by other  Forest a n d C a p i l a n o ) a p p e a r researchers  (Table  3), the  81 p r e d o m i n a n c e of Elaphomyces  in the collections m a y a c c o u n t for t h e s e higher  values. E. granulatus fruits primarily in the spring ( L u o m a et al. 1991), but c a n fruit at other times d e p e n d i n g on local conditions (Trappe 1976; C a s t e l l a n o et al. 1989). T h i s s p e c i e s g e n e r a t e s long-lasting truffles that are s l o w to mature a n d d e c a y a n d m a y persist in the substrate year-round (Hunt a n d T r a p p e 1987; L u o m a et al. 1 9 9 1 ; J o h n s o n 1994a). Truffle c o m m u n i t i e s d o m i n a t e d by s u c h long-lived s p e c i e s tend to exhibit m o r e regular s e a s o n a l standing c r o p s ( J o h n s o n 1 9 9 4 a ; North et al. 1997), w h i c h c o u l d explain the relatively consistent patterns of s e a s o n a l truffle production in the present study. G i v e n the variability in truffle fruiting in time a n d s p a c e reported in m a n y studies (e.g. F o g e l 1976; Hunt a n d T r a p p e 1987; L u o m a et al. 1991), completely d o c u m e n t i n g the o c c u r r e n c e of truffle s p e c i e s c a n be challenging a n d requires a long-term a p p r o a c h (Hunt a n d T r a p p e 1987). months (3,600 m  Despite intensive s a m p l i n g , after 2 9  cumulative area), C o l g a n (1997) w a s still encountering additional  2  truffle s p e c i e s on s o m e sites; Hunt a n d T r a p p e (1987) reported similar trends after 32 months (1,536 m months (4,304 m  2  2  cumulative area).  E l e v e n truffle s p e c i e s w e r e found after 21  cumulative area) in this study; it is p o s s i b l e that more s p e c i e s  might h a v e b e e n e n c o u n t e r e d if the study w a s e x t e n d e d . T o g e t h e r with the u s e of objective rules to locate plots a n d the application of a correction factor to a c c o u n t for differences in the non-productive a r e a a m o n g sites, the a p p r o a c h u s e d in this study e n a b l e d the calculation of a representative index of truffle production that w a s c o m p a r a b l e a m o n g the five sites.  T h i s m e a s u r e is a n  index b e c a u s e actual standing c r o p s a n d truffle production c o u l d not be d e t e r m i n e d . Truffle b i o m a s s could be overestimated by double-counting long-lived s p o r o c a r p s  82 that persist b e y o n d the s a m p l i n g interval (Vogt et al. 1992; North et al. 1997). Alternatively,  biomass  could  b e underestimated  d u e to d e c o m p o s i t i o n a n d  m y c o p h a g y (Hunt a n d T r a p p e 1987; L u o m a etal. 1 9 9 1 ; V o g t etal. 1992; C l a r i d g e et al. 1993b; North et al. 1997) a n d m i s s e d e p h e m e r a l s p e c i e s that m a y fruit a n d d e c a y outside of the s a m p l i n g s e s s i o n s (Vogt e r a / . 1992; North et al. 1997). Findings from the diet a n a l y s i s s u p p l e m e n t e d the results of truffle s a m p l i n g to provide a more c o m p l e t e picture of the h y p o g e o u s m y c o t a present at the study sites. U p to eight more fungal taxa w e r e present in the diets of northern flying squirrels than w e r e found during field s a m p l i n g at e a c h site; six of t h e s e taxa r e p r e s e n t e d major s e a s o n a l f o o d s .  T h i s d i s c r e p a n c y could b e partly d u e to e x t e n d e d intervals  b e t w e e n truffle s a m p l i n g a n d live trapping.  However, e v e n during  concurrent  surveys, northern flying squirrels c o n s u m e d o n a v e r a g e 1.9 times more truffle t a x a than w e r e found in the field.  C o l g a n (1997) reported similar results in Douglas-fir  forests of W a s h i n g t o n ; o n a v e r a g e 1.7 times m o r e g e n e r a w e r e c o n s u m e d by squirrels than w e r e collected by mycologists p e r s t a n d .  In eucalypt forests of  T a s m a n i a , bettongs (Bettongia s p p . ) a l s o found a n d c o n s u m e d 1.6 times  more  fungal taxa than t h o s e found within protective e x c l o s u r e s by collectors ( J o h n s o n 1994b).  A primary a s s u m p t i o n in this c o m p a r i s o n is that the effort a n d t e c h n i q u e  u s e d to s a m p l e truffles during e a c h s e s s i o n is appropriate for t a x a occurring at t h e time of s a m p l i n g . Truffle g e n e r a that w e r e not found o n the site but w e r e found in squirrel f e c e s within the s a m e time period w e r e a s s u m e d to b e u n c o m m o n or rare, consistent with J o h n s o n (1994b) a n d C o l g a n (1997).  Furthermore, the group of  f e c a l s a m p l e s collected in e a c h s e s s i o n a n d u s e d in dietary a n a l y s i s is a s s u m e d to represent the diet of squirrel populations at the time o n e a c h site; s m a l l s a m p l e s i z e s may  p o s e a limitation  to this  approach.  Differences  between  diet  a n d site  83 evaluations m a y b e d u e to s a m p l i n g (e.g. s a m p l i n g error, inadequate s a m p l e size) or squirrel foraging b e h a v i o u r (described  below).  It is unlikely that s a m p l i n g error is r e s p o n s i b l e for m i s s i n g truffles in the field. Prior to s a m p l i n g , field c r e w s w e r e s h o w n a variety  of truffle v o u c h e r s  from  collections throughout the Pacific Northwest, including s p e c i m e n s of a range of s i z e s , s h a p e s , colours, a n d textures.  C o l l e c t o r s carefully raked a n d sifted through  the organic layer a n d mineral soil by h a n d , locating the majority of truffles by feeling for fruitbodies e m b e d d e d in the organic layer or within c l u m p s in the mineral soil, and  o c c a s i o n a l l y by sighting  s p e c i m e n s that w e r e  uncovered  during  raking.  I n c o n s p i c u o u s fruitbodies might h a v e b e e n o v e r l o o k e d , but o u r s u c c e s s in finding Elaphomyces,  mature s p o r o c a r p s of w h i c h a r e e n c l o s e d in a dirt-encrusted  ( D o d g e 1929), m a k e s this explanation unlikely.  husk  In addition, although s o m e taxa  w e r e not found during concurrent s a m p l i n g at a particular time o n a particular site, s o m e of t h e s e s p e c i e s w e r e detected during g e n e r a l s a m p l i n g , thus validating the methodology for t h e s e t a x a . Inadequate s a m p l e s i z e m a y contribute to differences s e e n b e t w e e n diet a n d site evaluations. A n i n c r e a s e d s a m p l i n g effort would improve the representation of u n c o m m o n or rare s p e c i e s in truffle collections.  However, the a m o u n t of s a m p l i n g  during the primary collection period, including the f r e q u e n c y of visits a n d the total area  excavated  during  r e s e a r c h e r s (Table 8).  each  visit,  e x c e e d e d the s a m p l i n g  efforts  of  many  M e t h o d s u s e d w e r e a d e q u a t e to e n s u r e reliable, a c c u r a t e  data within the constraints i m p o s e d by a limited budget a n d time f r a m e a n d the experimental d e s i g n of a larger, related study ( R a n s o m e 2 0 0 1 ; R a n s o m e a n d Sullivan 2 0 0 2 , 2 0 0 3 , 2004).  84 Differences between truffle taxa in the diet and field could b e d u e to foraging by resident squirrels outside the study a r e a s .  H o w e v e r , live-trapping grids w e r e  e s t a b l i s h e d within a larger contiguous a r e a a n d w e r e s u r r o u n d e d by a buffer of similar forest at least 1 0 0 m wide.  A l t h o u g h not confirmed, this adjacent habitat  probably had similar truffle communities. S p e c i e s that are targeted for c o n s u m p t i o n by m y c o p h a g i s t s m a y b e m i s s e d or under-represented in field collections (Ure a n d M a s e r 1982; C l a r i d g e et al. 1993b; J o h n s o n 1994b; North et al. 1997), e s p e c i a l l y if they a r e rare or fruit infrequently (North et al. 1997).  R a t e s of m y c o p h a g y  c a n b e significant;  mycophagists  c o n s u m e d up to 9 9 % of the b i o m a s s of o n e u n c o m m o n truffle s p e c i e s in western hemlock forests of W a s h i n g t o n (North etal. 1997) and up to 7 0 % of truffle s p e c i e s in eucalypt forests of T a s m a n i a (Johnston 1994b).  C o n s u m p t i o n rates of 5 5 % a n d  8 7 % were recorded for s p e c i e s of Melanogasterand  Rhizopogon (North etal. 1997).  A s s u m i n g similar p r e f e r e n c e s , t h e s e significant rates of harvest could explain w h y t h e s e g e n e r a w e r e found in squirrel diets but not o n the site during  concurrent  s u r v e y s in the present study. Both of t h e s e g e n e r a w e r e present a s major s e a s o n a l f o o d s in this study. Finally, this d i s c r e p a n c y could b e attributed to a greater efficiency by northern flying squirrels at locating truffles c o m p a r e d to mycologists ( C o l g a n 1997), despite their rarity.  Efficiently locating a n d extracting truffles m a y b e e s s e n t i a l for northern  flying squirrels to avoid predation a n d m a x i m i z e energy g a i n s relative to the c o s t s of foraging ( C o l g a n 1997).  A d a p t a t i o n s , s u c h a s a k e e n s e n s e of s m e l l , e n a b l e  northern flying squirrels to detect odours emitted from mature truffles at c l o s e range (Pyare a n d L o n g l a n d 2001b).  Squirrels m a y u s e s o c i a l a n d visual c u e s (e.g.  p r e s e n c e of logs; P y a r e a n d L o n g l a n d 2001b) to locate foraging p a t c h e s .  In  85 addition, the t e n d e n c y for truffles to fruit in clustered ( F o g e l 1976; S t a t e s 1 9 8 5 ; V o g t e r a / . 1992) a n d perennial ( P y a r e a n d L o n g l a n d 2001b) patterns c r e a t e s predictable foraging  areas.  The  a s s o c i a t i o n of  northern  flying  squirrels  with  truffle-rich  microhabitats (Pyare a n d L o n g l a n d 2002) a n d radiotelemetry o b s e r v a t i o n s of their repeated visits to s u c h p a t c h e s over y e a r s ( C a r e y 2001) s u g g e s t s that northern flying squirrels m a y r e m e m b e r s u c h locations a n d be a b l e to find t h e m a g a i n ( P y a r e a n d L o n g l a n d 2 0 0 1 b , 2002). Squirrels w e r e selective in the s p e c i e s of fungi they c o n s u m e d in the present study.  T h e observation that rare truffle s p e c i e s w e r e c o n s u m e d a s major s e a s o n a l  f o o d s provides e v i d e n c e that squirrels are s e e k i n g out t h e s e specific fungi c o n s u m p t i o n rather than grazing a c c o r d i n g to fungal availability. although  not  Melanogaster  collected from  the  five  sites (i.e. d e e m e d  for  For example,  uncommon  or  rare),  w a s s e a s o n a l l y important in squirrel diets (Table 16) a n d 7 1 % of f e c a l  s a m p l e s collected at o n e site during o n e s e s s i o n contained Melanogaster  s p o r e s in  a m o u n t s s u g g e s t i n g it w a s a major food item (Figure 6 D ) . Particular truffle taxa m a y be s e l e c t e d for r e a s o n s including: e a s e of detection a n d extraction (e.g. truffle odour, s i z e , fruiting patterns, position in the substrate, a n d type of substrate) (Smith 1968; C o r k a n d K e n a g y 1989b; J o h n s o n 1994b); palatability ( F o g e l a n d T r a p p e 1978); s p o r o c a r p nutrient, energetic, or water content a n d digestibility (Vogt a n d E d m o n d s 1 9 8 1 ; G r o n w a l l a n d P e h r s o n 1984; C o r k a n d K e n a g y 1989b); previous a n i m a l e x p e r i e n c e ( G o s s e l i n a n d C h i a 1996); a n i m a l s e a r c h b e h a v i o u r a s s o c i a t e d with truffle distribution (e.g. c l u m p e d s p e c i e s ) ; predation risk (e.g. s p e c i e s that are a s s o c i a t e d with c o v e r a n d tend to fruit around the roots of s h r u b s or by logs) (Lima a n d V a l o n e 1986); a n d g e n d e r differences (e.g. s e n s o r y acuity of f e m a l e bettongs a p p e a r s to vary a c c o r d i n g to their reproductive condition) ( J o h n s o n 1994c).  86 P r e v i o u s r e s e a r c h e r s h a v e d e s c r i b e d northern flying squirrels a s 'obligate' (Hall 1991) m y c o p h a g i s t s , b a s e d o n the p r e d o m i n a n c e a n d diversity of fungal s p o r e s a n d relatively low o c c u r r e n c e of other major food  items in their  diet.  However, the p r e v a l e n c e of plant material in the year-round diet of flying squirrel populations  in the  present study s u g g e s t s a more flexible, generalist  feeding  strategy, p e r h a p s in r e s p o n s e to lower fungal diversity a n d the p r e d o m i n a n c e of Elaphomyces  in their habitat.  T h i s finding is consistent with a recent study in  temperate rain forests of S E A l a s k a , w h e r e squirrels ate truffles,  but  vegetation for c o n s u m p t i o n during snow-free periods ( P y a r e et al. 2002).  targeted Because  flying squirrels ate truffles less frequently a n d included fewer g e n e r a of truffles in their diet than reported in studies from W a s h i n g t o n , O r e g o n , a n d California, the authors c o n c l u d e d that the relationship b e t w e e n flying squirrels a n d truffles w a s w e a k e r in their study a r e a than had b e e n d o c u m e n t e d in the P a c i f i c Northwest ( P y a r e et al. 2002).  T h e ratio of plant material to fungal s p o r e s in this study w a s  e v e n more e x t r e m e than that reported by P y a r e et al. (2002), s o similar c o n c l u s i o n s are r e a s o n a b l e .  F r e q u e n c y a n d a b u n d a n c e v a l u e s of plant material are likely  conservative, s i n c e m a n y highly digestible plant parts s u c h a s s e e d s a n d berries c a n be under-represented or m i s s e d in f e c a l s a m p l e s (Thysell etal. 1997). s p o r e s of Elaphomyces  Interestingly,  d o m i n a t e d the fungal c o m p o n e n t of squirrels' diet ( P y a r e et  al. 2002), although a m y c o l o g i c a l survey w a s not c o n d u c t e d in their study a r e a to assess abundance. T h e long-lived Elaphomyces  is a year-round, d e p e n d a b l e food s o u r c e for  northern flying squirrels in this study, but E . granulatus h a s b e e n s h o w n to be low in digestible  energy  and  of  moderate  nutritional  (Claridge a n d C o r k 1994; C l a r i d g e et al. 1999).  quality  for  other  mycophagists  It is 'faintly aromatic' ( J o h n s o n  87 1994b) a n d m a y be less detectable or attractive to m y c o p h a g i s t s a s a c o n s e q u e n c e . Palatability (% c o n s u m e d by m y c o p h a g i s t s in o p e n plots, North et al. 1997) for this s p e c i e s w a s low (ca. 13%) relative to other taxa (e.g. up to 99%). T h e t e n d e n c y to form fruitbodies e m b e d d e d within thick, matted, well-rooted organic layers (North a n d G r e e n b e r g 1998) instead of in the top litter layer ( J o h n s o n 1994b) m a y i n c r e a s e handling time required to extract this truffle during harvest. Elaphomyces  T h i s m a y explain w h y  w a s often under-represented in the diet relative to its a b u n d a n c e in  the field. S p e c i e s of Elaphomyces  w e r e a l s o c o m m o n in eucalypt forests, but their  s p o r e s w e r e rare in the diet of bettongs in T a s m a n i a ( J o h n s t o n 1994b). T h e importance a n d n u m b e r of truffle taxa in the diet of northern  flying  squirrels a p p e a r e d to be highest in s u m m e r a n d fall. T h e s e s e a s o n s w e r e a l s o higher in overall n u m b e r of s p e c i e s found during truffle s a m p l i n g in the  primary  collection period. S i n c e only 12 f e c a l s a m p l e s w e r e e x a m i n e d from the s u m m e r of o n e y e a r (1997), interpretation  of g e n e r a l food habits for this s e a s o n s h o u l d be  m a d e with caution; however, M a s e r et al. (1986) s u g g e s t e d that 10 s a m p l e s w e r e a d e q u a t e to a c c o m p l i s h this task.  T h e p r e s e n c e of fungal taxa in the diet did  c o i n c i d e with known fruiting patterns; for e x a m p l e , Thaxterogster are known to fruit in the s u m m e r a n d fall ( C a s t e l l a n o et al. 1989) a n d a p p e a r s in the s u m m e r diet. T h i s pattern s u g g e s t s that northern flying squirrels m a y be s e a s o n a l l y opportunistic (Hall 1991) in their fungal c o n s u m p t i o n . c o n c l u s i o n ; they  noted  M a s e r et al. (1986) arrived at a similar  that c o n s u m p t i o n  patterns  of  northern  flying  squirrels  generally reflected known s e a s o n a l fruiting habits for m a n y truffle g e n e r a , although s o m e departures from this pattern w e r e o b s e r v e d . G i v e n that n u m e r o u s studies report truffles a s a major food of northern flying squirrels (Table 1) a n d s u g g e s t that differences in the s i z e of squirrel populations  88 a m o n g a r e a s might be d u e to differences in this fungal food r e s o u r c e ( R o s e n b u r g and Anthony  1992; W a t e r s a n d Z a b e l 1995; R a n s o m e a n d Sullivan 1997), I  e x p e c t e d to find densities of northern flying squirrels positively correlated with truffle production.  A  positive correlation  b e t w e e n the a b u n d a n c e of northern  flying  squirrels a n d truffles w a s found using four of the five sites in the a n a l y s i s . C a p i l a n o , w h i c h ranked first in m e a s u r e s of truffle production but fifth in a v e r a g e squirrel density, w a s markedly inconsistent with this a s s o c i a t i o n . S i n c e the m e a s u r e s u s e d to represent truffle a n d squirrel populations w e r e relevant, a c c u r a t e a n d valid, this result s u g g e s t s that the n u m b e r s of flying squirrels c a n n o t be e x p l a i n e d by truffle production a l o n e at the five sites. The  consumption  of  vegetation  by  squirrels  probably  confounds  the  relationship b e t w e e n truffle production a n d squirrel a b u n d a n c e . V e g e t a t i o n is a n important c o m p o n e n t of food r e s o u r c e s for northern flying squirrels a n d a s s u c h , s h o u l d be included in this a n a l y s i s ; it is p o s s i b l e that a combination of t h e s e two factors would provide a more consistent a s s o c i a t i o n .  In addition, although the  indices of truffle production reflect a m e a s u r e of a b u n d a n c e , this m a y not b e proportionate to availability. T h e availability of different fungal taxa to a c o n s u m e r is related to their accessibility ( J o h n s o n 1980), which c a n be affected by m a n y factors, s u c h a s s p e c i e s - s p e c i f i c fruiting patterns a n d substrates ( F o g e l 1976; A m a r a n t h u s et al. 1994; North a n d G r e e n b e r g 1998; P y a r e a n d L o n g l a n d 2002), food quality (e.g. digestibility; C o r k a n d K e n a g y 1989b), predation risk (Lima a n d V a l o n e 1986), a n d s o c i a l behaviour or a g e c l a s s (Boutin 1990).  T h e o c c u r r e n c e of northern flying  squirrels in live-traps h a s b e e n positively a s s o c i a t e d with microhabitats containing proximal vegetative c o v e r ( P y a r e a n d L o n g l a n d 2002), w h i c h could s e r v e a s both a s o u r c e of food a n d protection from predators.  C o n d u c t i n g a diet a n a l y s i s prior to  89 fieldwork to determine predominant food items m a y help to d e t e r m i n e  relevant  v a r i a b l e s for further study; however, quantifying the food a v a i l a b l e to a c o n s u m e r in a meaningful w a y c a n be difficult (Sinclair et al. 1 9 8 2 ; Boutin 1990). T h e effects of competition with other m y c o p h a g o u s a n i m a l s , s u c h a s D o u g l a s squirrels, m a y a l s o c o n f o u n d the relationship b e t w e e n truffle a n d northern flying squirrel a b u n d a n c e .  F o r e x a m p l e , the highest densities of D o u g l a s squirrels w e r e  found in C a p i l a n o ( R a n s o m e 2001); this c o u l d result in f e w e r northern flying squirrels than e x p e c t e d b a s e d o n the a b u n d a n c e of f o o d r e s o u r c e s .  Differential predation  rates a m o n g s t the five sites m a y a l s o impact squirrel d e n s i t i e s , further c o n f o u n d i n g the relationship b e t w e e n food supply a n d population s i z e .  90  CONCLUSIONS AND MANAGEMENT IMPLICATIONS  E l e v e n truffle s p e c i e s representing six g e n e r a w e r e collected at the five sites, with o n e major s p e c i e s , Elaphomyces  granulatus, predominating truffle collections.  A suitable index of fungal r e s o u r c e s w a s d e v e l o p e d from s y s t e m a t i c s a m p l i n g of truffle c o m m u n i t i e s .  N i n e additional truffle taxa w e r e d i s c o v e r e d in the diets of live-  trapped northern flying squirrels, w h i c h s u p p l e m e n t e d the results of truffle s a m p l i n g to provide a more c o m p l e t e picture of the h y p o g e o u s m y c o t a present at the five sites.  Plant material w a s a significant c o m p o n e n t of the year-round diets of live-  trapped northern flying squirrels.  Truffles represented s e a s o n a l l y important f o o d s .  T h e results s u g g e s t a more flexible, generalist feeding strategy than previously reported by other r e s e a r c h e r s in the Pacific Northwest. A c o m p a r i s o n of concurrent truffle a n d diet s u r v e y s indicated that s o m e truffles that w e r e u n c o m m o n - t o - r a r e in the field w e r e preferentially s e l e c t e d by northern flying squirrels for c o n s u m p t i o n . Densities of flying squirrels cannot be e x p l a i n e d by truffle production a l o n e at the five sites; a c o m b i n a t i o n of vegetation a n d truffle i n d i c e s w o u l d provide a m o r e meaningful representation of food r e s o u r c e s . R e p r o d u c t i v e s u c c e s s (White 1 9 9 6 ; T h o m e et al. 1999) a n d survival during juvenile d i s p e r s a l (Miller et al. 1997) of northern spotted owls h a v e b e e n positively a s s o c i a t e d with prey a b u n d a n c e .  M e a s u r e s to e n h a n c e populations of northern  flying squirrels could therefore aid in the m a n a g e m e n t of the northern spotted owl ( C a r e y et al. 1 9 9 2 ; R a n s o m e 2001). related  study,  squirrels w e r e  R a n s o m e (2001) strongly  U s i n g a n experimental a p p r o a c h in a larger  c o n c l u d e d that populations  influenced  by the availability  of northern  of f o o d .  flying  T h e positive  relationship b e t w e e n densities of northern flying squirrels a n d production of truffles  91 in four of the five sites in this study is consistent with this conclusion. 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Truffle g e n e r a and type found at e a c h site during o n e to 4 s e s s i o n s from M a y 1997 to F e b r u a r y 1998 a n d o n e c a n c e l e d s e s s i o n in F e b r u a r y 1999. Site Genus  Type  Elaphomyces  A  Hydnotrya  A  Rhizopogon  B  Total g e n e r a  3  CAP  CHEH  COQ  RF  SDF  X  X  X  X  X  X  X  X  X 2  X 2  Total s e s s i o n s 4 2 A = Ascomycotina, B = Basidiomycotina, Z = Zygomycotina s e e Tables 6 and 7 for number of plots sampled 6  3  2  1  4  5  3  each  session.  a  b  within  Appendix 2. The occurrence of each genus of truffle in the diet of northern flying squirrels (shaded) and found during truffle sessions (x) at the five study sites.  HYST LEUP LEUG MELA OCTA PICO RHIZ RUSS THAX TUBE UNKN Truffle session N (fecal samples)  Sept.  X  X  X  X  X  3  Dec.  ~>  Oct.  Apr.  Mar.  X  Feb.  X  Jan.1998  Nov.  3  —}  Sept.  Jun.  May  Apr.  Mar. 1997  Dec.  —>  Nov.  3  Sept.  COQ  May  Mar.  Feb.1998  3 -J  Nov.  Jun.  X  May  X  Mar.  Dec.  X  3  Feb.1997  —)  Sept.  X  Jun.  X  CHEH  Apr.  Feb.1998  X  Mar.  Nov.  July  X  Sept.  CHAM ELAP ENDO GENE HYDN  May  3  Apr.  Taxa  Mar. 1997  (: A P  —  X  X  •  X  X  X  X  X  X  X  X  X  X  X  X X  X  X  i .v. X  1  5  X  X  X  X  X  X  0  0  3  0  5  X  5  0  0  X  X  X  0  0  0  X  3  5  5  4  X  3  5  108  1 3  6  X  X  X  0  0  0  X  4  0  5  5  4  X  X  X  X  X  0  0  0  5  X  9  0  5  X  X  0  0  X  0  7  0  109  (continued)  Nov.  Sept.  Jun.  Apr.  Nov.  Jun.  May  cn £ > LOil_  Apr.  Dec.  Nov.  3 -5  Sept.  Apr.  o>  Mar.  SDF  Feb.  Jan.1998  <D  Dec.  u.  Jun.  Taxa  Apr.  ri 9  Mar.  c cn n  Sept.  RF  Jan.1998  Appendix 2.  CHAM jjji X X X X x x X X X X X X ELAP X ENDO GENE X n X HYDN HYST LEUP LEUG i MELA liiii OCTA PICO X X RHIZ RUSS THAX X TUBE X UNKN Truffle X X X X X X X X X X X X X session N (fecal 1 2 5 1 0 5 5 3 0 0 0 1 0 5 5 5 4 6 9 1 1 0 0 6 samples) 2 3 CHAM = Chamonixia; ELAP = Elaphomyces; ENDO = Endogone, GENE = Genea; HYDN = Hydnotrya; HYST = Hysterangium, LEUG = Leucogaster, LEUP = Leucophleps; MELA = Melanogaster, OCTA = Octavianina; PICO = Picoa; RHIZ = Rhizopogon; RUSS = Russulaceae; THAX = Thaxterogaster, TUBE = Tuber, UNKN = Unknown immature sporocarp. 8  

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