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Gut-retention time in mycophagous mammals: a review anda study of truffle-like fungal spore retention in the swampwallaby

Melissa A. DANKS*

Ecosystem Management, University of New England, Armidale, New South Wales 2351, Australia

a r t i c l e i n f o

Article history:

Received 28 February 2011

Revision received 11 July 2011

Accepted 13 July 2011

Available online 2 October 2011

Corresponding editor:

Jeff Powell

Keywords:

Forest ecology

Gut-passage

Marsupials

Mean retention time

Mycophagy

Mycorrhizas

Spore dispersal

Truffles

a b s t r a c t

Variation in the gut-retention time of macrofungal spores influences the distance to which

spores are dispersed by mycophagous (fungus-feeding) mammals and is of interest in

examining mammal-fungal interactions. In reviewing published studies of fluid and

particle (including macrofungal spore) digesta gut-retention times in ground-dwelling

mycophagous mammals, weighted mean retention times (MRT) were found to range

6.6e55.5 hr. Among macropodoid marsupials, fluid and small particle weighted MRT was

longer in mycophagous species than non-mycophagous species but statistical support for

this difference was weak (estimated mean difference 7.2 hr; 95 % CL [�0.8, 15.1] hr). Gut-

retention of truffle-like (below-ground fruiting) fungal spores was examined in the

swamp wallaby (Wallabia bicolor), a browsing macropodid marsupial that regularly eats

macrofungal fruit-bodies. Two wallabies of different body weights were examined in

a captive feeding trial. MRT of marker spores were 26.9 hr and 35.1 hr for the larger and

smaller animal respectively. A small number of marker spores were found in faecal pellets

up to 69 hr after ingestion, suggesting that there is potential for long distance dispersal of

fungal spores by swamp wallabies. The studied swamp wallabies probably carry fungal

spores for similar times to smaller mycophagous marsupials, including the strongly

mycophagous potoroids. Further studies of spore gut-passage, including MRT, in

mycophagous mammals would help clarify differences among species and groups of

species.

ª 2011 Elsevier Ltd and The British Mycological Society. All rights reserved.

Introduction

Interactions between mycorrhizal fungi, host plants, and

mammals influence forest ecosystem function. Trees and

other woody plants form biotrophic symbioses with ectomy-

corrhizal (EM) fungi (Brundrett 1991; Read 1991). Most EM fungi

produce fruit bodies (sporocarps) and these are an important

food resource for many mammals (Fogel & Trappe 1978;

Claridge & May 1994; Claridge et al. 1996; Maser et al. 2008).

Mammals are vital spore dispersal agents, particularly for

truffle-like (below-ground fruiting) sporocarpic fungi that do

not actively discharge their spores (Fogel & Trappe 1978;

Claridge & May 1994; Claridge et al. 1996; Johnson 1996;

Reddell et al. 1997; Bougher & Lebel 2001; Maser et al. 2008).

Spore dispersal is important for both maintenance of genetic

flow within and between fungal populations and for coloniza-

tion of new habitats (Bruns et al. 2009). For mycorrhizal host

plants and the plant-soil system, maintenance of a diverse

* Tel.: 61 424726667.E-mail address: mdanks@une.edu.au

available at www.sciencedirect.com

journal homepage: www.elsevier .com/locate/ funeco

1754-5048/$ e see front matter ª 2011 Elsevier Ltd and The British Mycological Society. All rights reserved.doi:10.1016/j.funeco.2011.08.005

f u n g a l e c o l o g y 5 ( 2 0 1 2 ) 2 0 0e2 1 0

Author's personal copy

mycorrhizal fungal community maintains resilience through

resource partitioning and competition amongst fungi (Perry

et al. 1989; Deacon & Fleming 1992; Bruns 1995). Rapid

seasonal turnover of plant root tips results in strong local-scale

competition among mycorrhizal fungi for this resource (Bruns

1995). By disseminating spores in their faecal pellets, mycoph-

agous (fungus-feeding) mammals help maintain fungal diver-

sity within their home range (Maser et al. 2008). While most

mycophagousmammalmovement occurswithin a frequently-

used area (home range), occasional long distance movements

occur and may be significant spore dispersal events.

Few mycophagous mammals remain on the New England

Tableland of north-eastern New South Wales; bettongs,

potoroos, and bandicoots have largely been extirpated from

the modified landscapes of this region in the period since

European occupation (Jarman & Vernes 2006). However, the

swamp wallaby, Wallabia bicolor, a plant browser and regular

mycophagist is resilient in these EM-forested landscapes.

Swamp wallabies consume a diversity of truffle-like fungi

year-round (M. Danks, unpublished data; Claridge et al. 2001;

Vernes & McGrath 2009; Vernes 2010) and may contribute to

the maintenance of vital mammal-truffle-plant relationships

in these simplified communities.

Gut-retention time of fungal spores in mycophagous

mammals is of interest in examining mammal-fungal inter-

actions as, along with movement patterns, variation in gut-

retention influences the distance to which spores may be

dispersed (Cork & Kenagy 1989b). Gut-passage is influenced by

body mass, gut morphology and diet (Cork & Kenagy 1989b;

Hume 1989). Most studies examining mammalian digesta

passage have held study animals in metabolism cages and

used chemical or physical markers to illustrate the passage of

fluid or particle digesta phases (e.g. Calaby 1958; Warner

1981a; Hume & Carlisle 1985; Sakaguchi & Hume 1990; Moyle

et al. 1995; McClelland et al. 1999; Gibson & Hume 2000; Pei

et al. 2001). Gut-passage has rarely been studied in free-

ranging mammals on a natural diet, making it problematic

to interpret the ecological meaning of reported gut-retention

times. Gut-retention time of fungal spores has also received

relatively little attention. The few studies that have directly

assessed gut-retention of fungal spores have examined

mycophagous rodents; for example, the giant white-tailed rat,

Uromys caudimaculatus (Comport & Hume 1998), the golden-

mantled ground squirrel, Spermophilus saturatus, and the

deer mouse, Peromyscus maniculatus (Cork & Kenagy 1989b).

The present study is the first to assess spore gut-passage in

a mycophagous mammal on a semi-natural diet, and the first

to measure spore gut-passage in a macropodoid marsupial.

In this paper I: (1) review published data on gut-retention

times in mycophagous mammals, including macropodids

(wallabies), potoroids (potoroos and bettongs), peramelids

(bandicoots), rodents (squirrels, voles, andmice), and possums;

and (2) examine the time taken for native truffle-like fungal

spores to pass through the gut of swamp wallabies. I use gut-

retention times to broadly examine the spore dispersal role of

these mammals rather than to compare their digestive effi-

ciency. Factors influencing digesta passage are discussed in

relation to fluid, small particle, and macrofungal spore gut-

retention time in the swamp wallaby and other mycophagous

mammals. Fluid and particulate digesta pass through the

digestive tract as different digesta phases (Faichney 1975).

Spores of EM fungi are thought, due to their small size of

generally <20 mm diameter, to move through the gut with the

fluid phase although some spores may remain attached to

sporocarp fragments and pass through the gut with the large

particlephase (Comport&Hume1998).Sporegut-retention time

in the swampwallaby is expected to bemost similar to fluidgut-

retention times reported for other browsing and grazing

wallabies as, despite their smaller size, these animals are most

similar to swampwallabies in termsofdietandgutmorphology.

Materials and methods

Published data on digesta gut-passage in mycophagousmammals

Published data on macrofungal spore, fluid, and particle

digesta mean retention times (MRT) in mycophagous

mammals were collated. Comparisons among macropodoid

marsupials (macropodids e kangaroos and wallabies; and

potoroids e potoroos, bettongs and rat-kangaroos), both

mycophagous and non-mycophagous, were also made. The

50 % excretion time (ET) measure, while not the same as MRT,

is considered similar enough for broad comparisons of gut-

retention times to be made (Stevens & Hume 1995), so 50 %

ET measures were included in this summary where MRT was

not reported. Both measures are referred to here as ‘gut-

retention time’. Several researchers provide information on

digesta passage in mycophagous mammals but do not report

MRT or 50 % ET (e.g. Calaby 1958; Hume & Carlisle 1985;

Richardson 1989), preventing comparison with the present

study, so these studies were not included in the summary.

In studies of large particle (size ranges between

300e1200 mm diameter) MRT, various chemical or radio-

isotope markers, including chromium mordanted onto cell-

wall constituents (Cr-CWC), dyed leaf particles, and 103Ru-

labelled tris-(1,10 phenanthroline)-ruthenium (11) chloride

(Ru-P) leaf particles were utilised. Fluid digesta MRT was

assessed using either cobalt-ethylenediamine tetra-acetic

acid (Co-EDTA), or the 51chromium complex of ethylenedi-

amine tetra-acetic acid (Cr-EDTA). The marker used can

influence the measured rate of passage of digesta. For

example, Ru-P migrates from large to small digesta particles

within the gut of sheep (Faichney & Griffiths 1978; Egan &

Doyle 1984) and macropods (Freudenberger & Hume 1992) so

that MRT of large particles may be underestimated using this

marker. Cr-EDTA may not completely associate with the fluid

phase (Faichney 1975), while Co-EDTA associates almost

exclusively with fluid (Ud�en et al. 1980). Additionally, the fibre

content and particle size distribution of the experimental diet,

frequency of feeding, and animal activity levels will also

influence digesta gut-passage and thereforemeasures of MRT.

Sakaguchi & Hume (1990) reported small (<75 mm diameter)

particle MRT and compared passage with that of fluids and

larger (300e600 mm) particles. The fine particles passed

through the gut with the fluid digesta phase. Therefore, I have

assumed measures of fluid digesta passage to be measures of

the passage of both solutes and small particulate digesta

(<75 mm).

Gut-retention time in mycophagous mammals 201

Author's personal copy

For the purpose of drawing broad comparisons among

mycophagous mammal species, weighted average MRT esti-

mates were calculated for each animal species (weighted by

original study sample size) and group of species (weighted by

the number of sources), based on mean MRT values reported

for those species on a range of experimental diets and varying

methodology. To compare average MRT between mycopha-

gous and non-mycophagous macropodoid marsupials, 95 %

confidence limits were calculated around the estimatedmean

difference between these groups. Sample size was generally

small (range 1e13 animals per experiment) and the number of

sources per species ranged between one and nine. Related

information including trophic classification, body mass,

and presence of selective gut-retention mechanisms was

summarised.

Swamp wallabies

Swamp wallabies were trapped in eucalypt woodland at

Newholme Field Station, northern New SouthWales, Australia

in Jun. 2009, and housed in large (1e1.2 ha) naturally vegetated

(eucalypt woodland) pens on site. Four purpose-built soft-

walled wallaby traps, 700 mm� 1200 mm� 700 mm, based on

the design of Di Stefano et al. (2005) were baited and set late

each afternoon, and checked early the following morning, for

three consecutive nights. Trapping to source animals for the

feeding trial was limited to three consecutive nights to mini-

mise the time for which animals would be held prior to

commencing the feeding trial, and only adults in good condi-

tion and without pouch young or young-at-foot were selected

for the feeding trial. Two wallabies were used in this study;

both were adult males and each weighed 21 kg and 10 kg

respectively. Lucerne hay, pelleted feed and apple pieces were

provided as supplementary feed throughout, although

wallabies were observed to browse on shrubs and grasses.

Duringanacclimationperiod of 3 d, fresh faecal pelletswere

regularly collected and samples examined microscopically for

the presence of macrofungal spores. A �1 cm3 portion was

taken from each pellet-group. Sub-samples (0.5 g) were rehy-

drated in 10 ml water for 1 hr, macerated, and washed through

a 50 mm� 50 mmsievewith a further 20 mlofwater. The sample

was then centrifuged and the supernatant removed by pipette

until 2 ml remained. The remaining sample was thoroughly

mixed and three drops placed on a slide with one drop of

Melzer’s Reagent. Melzer’s Reagent produces colour reactions

that aid identification of some fungi. Slideswere systematically

scanned at �400 magnification with an Olympus CX41 light

microscope (Fig 1A). Magnification of�1000 was used to clarify

spore morphology to aid identification. It was essential to

determine an appropriate fungal ‘marker’ taxon thatwas easily

found in the environment, but not currently in the diet of the

swamp wallabies in the pen area. Austrogautieria clelandii was

selected as amarker for this trial because (1) it was not found in

faecal pellets of the captured wallabies during the acclimation

period, (2) it is known to occur and be consumed by swamp

wallabies at nearby sites (M. Danks, unpublished data), (3) it is

easily identifiedby itsdistinctivesporemorphology (Fig 1B), and

(4) it was readily available in a quantity suitable for this study.

After theacclimationperiod, thewallabieswere recaptured, fed

(by use of a syringe to the back of themouth) a 10 ml pulse dose

of slurry ofA. clelandii sporocarps, and released back to the pen.

The dose was delivered as a slurry to ensure ingestion of

a standard quantity of spores (equivalent to approximately two

large sporocarps) at a known time. Swampwallabies were held

for a further 4 ½ d and then released. Wallaby capture and

handling protocol followed guidelines of the American Society

of Mammalogists (Gannon et al. 2007) and was approved by the

Animal Ethics Committee at the University of New England

(code AEC09-023).

Gut-passage of macrofungal spore digesta

Prior to dosing wallabies with the spore slurry, three transects

perpen (totalling5 %ofpenarea)weremarkedandclearedofall

Fig 1 e (A) EM of fungal spores in swamp wallaby faecal

pellet during acclimation period (pellet material stained

with Melzer’s Reagent to aid identification of some groups

of fungi). (B) Distinctive ridged spores of Austrogautieria sp.

in swamp wallaby faecal pellet collected after oral dosing

with Austrogautieria sp. sporocarp slurry. Inset:

Austrogautieria sp. spores from fresh sporocarp, showing

side and end view of spores. Micrographs taken at 4003

magnification (Inset micrograph taken at 10003

magnification). Bar scale for all images 10 mm.

202 M.A. Danks

Author's personal copy

faecal pellets. Faecal pelletswere collected fromthese transects

for 4 ½ d following dosing (4 hourly for 48 hr, then 6 hourly for

the next 36 hr, and then 12 hourly for a further 24 hr). Faecal

material was oven-dried (40 �C for 12e24 hr) and bulked by

collection period. Samples were processed for microscopic

examination as described earlier, omitting Melzer’s Reagent,

which was not necessary to distinguish marker spores. Slides

were examined at 400� magnification and the number of

marker spores in 30fields-of-view counted. Amounts ofmarker

excreted were expressed as proportions of the total number of

marker spores seen in faecal samples. ETs were estimated as

the mid-point of each collection period. Overall (dose to excre-

tion) mean retention time (MRT), the average time taken for

a marker particle to be excreted after a pulse dose, was calcu-

latedbyuseof the formulaP

(Miti)/P

MiwhereMi is theamount

of marker excreted in the ith defecation at time ti (Blaxter et al.

1956) as recommended byWarner (1981b).

Results

Digesta gut-passage in mycophagous mammals

Previous researchers specifically examining macrofungal

spore gut-passage examined mycophagous rodents with

mean body mass of 15e660 g and reported spore MRT of

12e48.4 hr. Studies of fluid (and small particle) and large

particle digesta marker passage in mycophagous macro-

podids, potoroids, peramelids, phalangerids, and rodents re-

ported fluid and particle marker MRT or 50 % ET of 6e71 hr.

WeightedMRT for fluid and small particles was shortest in the

red-necked pademelon Thylogale thetis (12 hr) and longest in

the brushtail possum Trichosurus vulpecula (47.4� 5.5 hr;

Table 1). Weighted MRT for large particles ranged from 6.6 hr

in the meadow vole Microtus pennsylvanicus to 49.1 (�9.5) hr in

the brushtail possum.

Digesta gut-passage in macropodoid marsupials

Among macropodoid marsupials, weighted MRT for fluid and

small particles (including macrofungal spores) ranged from

12 hr in the small browsing red-necked pademelon to 31 hr in

both the swamp wallaby and the small omnivorous rufous

bettong Aepyprymnus rufescens (Table 1). Fluids and small

particles including macrofungal spores were retained for

longer by mycophagous macropodoids (24.3 [14.4, 34.2] hr;

weighted mean [lower 95 % CL, upper 95 % CL]) than by non-

mycophagous macropodoids (17.6 [13.8, 20.5] hr), although

statistical support for a mean difference was weak (7.2 [�0.8,

15.1] hr: mean difference, [lower 95 % CL, upper 95 % CL]).

There was no support for a mean difference in large particle

MRT between the two groups (mycophagous 29.2 [19.1, 39.2]

hr; non-mycophagous 31.8 [25.6, 38] hr; mean difference 2.6

[�6.4, 11.6] hr).

Passage of fungal spore marker through swamp wallaby gut

Patterns of excretion of marker spores over time were similar

but the timing of excretion differed slightly between the two

animals (Fig 2). The marker spores were first found in the

faecal pellets of the 21 kg and 10 kg animals at 6 hr and 22 hr,

andwere last seen at 63 hr and 69 hr respectively (Fig 2A). MRT

of spores was 27 hr and 35 hr, and modal retention time was

22 hr and 43 hr respectively. Fifty percent of themarker spores

were eliminated from the gut of both animals within 34 hr

(21 and 34 hr) and 90 % were eliminated within 51 hr (46 and

51 hr) after ingestion (Fig 2B).

Discussion

Fungal spore retention time in the swamp wallaby gut

This is the first study to examine digesta passage rate in the

swampwallaby, one of the few studies using a natural dietary

marker (macrofungal spores) to assess gut-retention time, and

one of the few studies to determine gut-retention time for

animals kept under semi-natural conditions. My results

suggest that the swamp wallabies sampled can carry ingested

spores for a mean 27e35 hr and some spores for up to 3 d. In

studies of smaller mycophagous mammals (potoroids and

rodents), spores remain viable after passage through the gut

(Kotter & Farentinos 1984; Lamont et al. 1985; Cork & Kenagy

1989a; Claridge et al. 1992; Caldwell et al. 2005). I therefore

assume that spores do not lose viability on dissemination in

swamp wallaby faeces and that swamp wallabies contribute

to effective dispersal of these spores. Swampwallabies occupy

home ranges 3e86 ha in size (M. Danks unpublished data;

Edwards & Ealey 1975; Troy & Coulson 1993; Di Stefano 2010;

Di Stefano et al. 2011) and so have the potential to disperse

spores across large areas. Occasional longer-distance move-

ments beyond the home range are also potentially significant

spore dispersal events.

Digesta gut-passage in macropodoid marsupials

Macropodoid marsupials are almost all foregut fermenters;

they have an enlarged forestomach, the principal site of

microbial digestion, made up of several regions, and a simple

hindgut (Langer 1980; Langer et al. 1980; Hume 1982). With

increasing body mass, the tubiform region of the forestomach

tends to increase in size and the sacciform region of the for-

estomach tends to decrease in size (Hume 1984). This trend is

explained by the ability of larger animals to utilise a more

fibrous (lower quality) diet; sincemetabolic requirements scale

with body size large animals require less energy relative tobody

mass thando small animals (Demment&Soest 1985). Anotable

exception to this trend is the rufous hare-wallaby, which

despite being small (1 kg; similar in size to the small potoroids),

has a high-fibre grazing diet and ‘kangaroo-like’ stomach

morphology (Bridie et al. 1994). The rufous hare-wallaby offsets

the disadvantages of small size on a high-fibre diet with low

food intake, discontinuous feeding, and a long distal colon for

storageof faeces, resulting in relatively longgut-retentiontimes

and thusmoreefficientdigestionofhigh-fibre food items (Bridie

et al. 1994). Digesta passes through the predominantly tubiform

stomach of the larger kangaroos relatively quickly (Hume 1984)

while in the potoroids the sacciform forestomach acts as

a storage chamber and fermentation site increasing the overall

rate of passage of digesta (Freudenberger et al. 1989).

Gut-retention time in mycophagous mammals 203

Author's personal copy

Table

1e

Overa

ll(dose

toexcretion)weightedm

eanretentiontim

e(M

RT,h)offluid

(solutesandsm

allparticles<

75mm

diam

eter),m

acrofu

ngalsp

ores(<

40mm

diam

eter),andlarg

eparticles(300e1200mm

diam

eter,

orunreported)in

(a)non-m

yco

phagousm

acropodoid

marsupials

(fam

iliesMacropodidaeandPotoro

idae),(b)

myco

phagousm

acropodoid

marsupials,and(c)so

meoth

erknownm

yco

phagousm

am

mals

WeightedMRT�1SE(h)

Taxa

Family

Tro

phic

Selective

gut-retention

Bodymass

(g)

Fluid

&sm

all

particle

nMacrofu

ngal

spore

nLarge

particle

nSource

(a)Non-m

yco

phagousmacropodoid

marsupial

Lago

rchesteshirsu

tus,

rufoushare-w

allaby

Macropodidae

H.graze

1190

23.4

1e

e38

1(Bridie

etal.1994)

Macrop

useu

genii,tammarwallaby

Macropodidae

H.graze

4800

13.6

�1.1

e4

ee

23.1

�2.2

e4

(Warn

er19

81a;Dellow

1982

)

Macrop

usgiga

nteus,

eastern

greykangaro

oMacropodidae

H.graze

20800

14.4

e1

ee

34.8

�4.3

e3

(Forb

es&

Tribe1970;

Dellow

1982)

Macrop

usrobustuserubescens,

euro

Macropodidae

H.graze

18200

18.6

�0.8

g3

ee

26.0

�2.0

g3

(Freudenberger&

Hume1992)

Macrop

usrobustusrobustus,

common

wallaro

o

Macropodidae

H.graze

20125

19.3

�0.4

e,g

4e

e30.1

�1.3

e,g

4(D

ellow

1982;

Freudenberger&

Hume1992)

Macrop

usrufus,

redkangaro

oMacropodidae

H.graze

25800

16.0

h2

ee

36.7

�2.5

i9

(Foot&

Romberg

1965;

McIntosh

1966;Forb

es&

Tribe1970;Munn&

Dawso

n2006)

Mean

17.1

[13.8,20.5]

31.8

[25.6,38.0]

(b)Myco

phagousmacropodoid

marsupial

Potorou

stridactylus,

long-n

ose

dpotoro

oPotoro

idae

M955

24.0

d2

ee

25.0

d2

(Wallis

1994)

Bettongiapen

icillata,woylieorbru

shtail

bettong

Potoro

idae

M1062

27.0

d2

ee

33.5

d2

(Wallis

1994)

Aep

yprymnusrufescen

s,ru

fousbettong

Potoro

idae

O2984

31.0

d2

ee

35.5

d2

(Wallis

1994)

Thylog

ale

thetis,red-n

eck

edpademelon

Macropodidae

H.bro

wse

4050

12.0

d,e

2e

e22.4

d,e

2(D

ellow

1982)

Wallabia

bicolor,sw

ampwallaby

Macropodidae

H.bro

wse

10000e21000

ee

31.0

f1

ee

This

study

Mean

24.3

[14.4,34.2]

29.2

[19.1,39.2]

(c)Oth

ermyco

phagousmammal

Perom

yscu

smaniculatus,

deermouse

Muro

idea

O15e19

ee

12.0

a1

10.3

1(C

ork

&Kenagy1989b)

Microtuspen

nsylvanicus,

meadow

vole

Muro

idea

H30e40

ee

ee

6.6

b2

(YoungOwl&

Batzli1998)

Uromys

caudim

acu

latus,

giantwhite-

tailedrat

Muro

idea

OLargeparticle

660

45.4

148.4

c1

55.5

1(C

omport

&Hume1998)

Eutamiasamoenus,

yellow-p

inech

ipmunk

Sciuridae

OLargeparticle

62

12.7

1e

e14.1

1(H

umeet

al.1993)

Spermop

hilussa

turatus,

golden-m

antled

gro

undsq

uirrel

Sciuridae

M216e327

ee

24.8

a1

24.1

1(C

ork

&Kenagy1989b)

Marm

otacaliga

ta,hoary

marm

ot

Sciuridae

HLargeparticle

2308

24.8

1e

e28.9

1(H

umeet

al.1993)

Isoodon

macrou

rus,

northern

bro

wn

bandicoot

Peramelidae

OFluid

250e3000

27.4

2e

e18.5

2(M

cClellandet

al.1999)

Perameles

nasu

ta,long-n

ose

dbandicoot

Peramelidae

OFluid

800e1000

28.4

d2

ee

17.5

d2

(Moyle

etal.1995)

Trichosurusvulpecula,co

mmonbru

shtail

possum

Phalangeridae

H.foliage

2350

47.4

�5.5

d4

ee

49.1

�9.5

d3

(Wellard

&Hume1981;

Foley&

Hume1987;

Sakaguch

i&

Hume1990)

204 M.A. Danks

Author's personal copy

Relatively little is known about swamp wallaby digestive

physiology, although some generalisations can bemade based

upon comparative gut morphology and diet habit. Gut

morphology is most similar to that of smaller wallabies; fore-

stomach and caecum (hindgut) structure are similar to that of

the tammar wallaby, a small (5 kg) grazer, and the red-necked

pademelon, a small (4 kg) browser (Dellow1979). The regionsof

the swamp wallaby gut are therefore expected to contribute

similarly to total stomach capacity (sacciform forestomach

30e51 %, tubiform forestomach 40e56 %, hindstomach

10e15 %; Dellow & Hume 1982) and the stomach to contribute

similarly to total gut capacity (76 %; Dellow&Hume 1982) as in

these two species and so account for similar proportions of

overall gut-retention times. The medium-sized, browsing

(low-fibre diet) swampwallaby has a forestomachmorphology

intermediate to the predominantly sacciform forestomach of

the small potoroids (low-fibre diets) and the predominantly

tubiform forestomach of the large grazing (high-fibre diets)

kangaroos (Stevens & Hume 1995). Osawa & Woodall (1992)

noted the similar gross anatomy of the swamp wallaby and

tammarwallaby intestinal tracts. The swampwallaby hindgut

(caecum) and large intestine are relatively small and simple

compared to the larger grazing kangaroos, most similar in

relative size and structure to that of the red-necked pademe-

lon, and consistent with a browsing, low-fibre diet (Osawa &

Woodall 1992). Osawa & Woodall (1992) also observed that

relative to body mass, the swamp wallaby small intestine is

longer while the large intestine is shorter than that of the red-

necked pademelon. Based on gut morphology and diet, reten-

tion timeoffluidsandsmall particles in the swampwallabygut

would be expected to be intermediate to the potoroids and the

large kangaroos, andmost similar to other browsingwallabies.

This prediction was not supported in the studied swamp

wallabies. The gut-retention time of truffle-like fungal spores

in the studied swamp wallabies is most similar to fluid gut-

retention times recorded for the smaller potoroids and per-

amelids despite great differences in body size and some

differences in gut morphology. The contribution of the small

intestine, although a small proportion of overall gut length,

might account for the longer than expected spore gut-

retention time in the study swamp wallabies.

Macropodoids exhibit differential digesta flow. Tubular

flow of digesta in the forestomach causes fluid and small

particle digesta to be expressed through the large particle

digesta, which remain longer in the forestomach formicrobial

fermentation resulting in longer overall gut-retention time of

large particles (Dellow 1982). The extent of digesta phase

separation is greater in the large kangaroos than in the small

wallabies and the potoroids (Dellow 1982; Hume 1989; Wallis

1994). In the larger kangaroos, differences between fluid and

large particle digesta range between 7 and 13 hr, compared to

10 hr in the small wallabies and 1e6 hr in the potoroids. In the

potoroid gut, fluid and particle digesta may pass through at

similar rates (Wallis 1994), although earlier radiographic

studies of digesta flow observed digesta phase separation

(Hume & Carlisle 1985; Richardson 1989). Of the peramelids

(hindgut fermenterswith a relatively simple forestomach), the

northern brown bandicoot Isoodon macrourus (McClelland et al.

1999) and the long-nosed bandicoot Perameles nasuta (Moyle

et al. 1995) selectively retain fluid and small particle digesta

Mean

33.4

[21.8,44.9]

26.9

[12.5,39.7]

Meanmyco

phagous

26.9

[20.0,33.7]

26.5

[17.7,35.3]

Meanmacropodoid

21.0

[16.4,25.5]

31.0

[26.5,35.3]

MeanMRT(�

1SE,w

here

n>3),weightedbysa

mple

size

,calculatedforsp

eciesacross

experimentald

iets.G

roupMRT[lower95%

confidence

limit,u

pper95%

confidence

limit],weightedbynumberof

sources.

MRTca

lculatedasreco

mmendedbyW

arn

er(1981b),exce

ptwhere

indicated.Bodymass:mean,orrangeifneithermeannorraw

valuesreported,ofstudyanim

als.

Tro

phic:H¼herb

ivore;O¼omnivore;M

¼primarily

myco

phagous.

n¼sa

mple

size

(numberofMRTestim

ates).

aMacrofu

ngalsp

ore

mark

er:

Elaphom

yces

granulatus.

bEstim

atedvisuallyfrom

graphedresu

lts.

cMacrofu

ngalsp

ore

mark

er:

Pisolithussp

.

dLargeparticle

mark

er:

Ru-P

(Dellow

1982;W

ellard

&Hume1981;Foley&

Hume1987;W

allis

1994).

eDellow

(1982):measu

redasmean50%

ET.MRTca

lculatedusingth

emeth

odofFaichney(1975)yieldedsimilarresu

lts.

fMacrofu

ngalsp

ore

mark

er:

Austroga

utieria

clelandii.

gCalculatedusingth

emeth

odofFaichney(1975).

hMunn&

Dawso

n(2006)only.

iFoot&

Romberg

(1965);McIntosh

(1966);Forb

es&

Tribe(1970):MRTca

lculatedusingth

emeth

odofCastle

(1956).

Gut-retention time in mycophagous mammals 205

Author's personal copy

in the hindgut while greater bilbies Macrotis lagotis do not

(Gibson & Hume 2000). Some (but not all) of the rodents also

selectively retain fluid and small particles in the hindgut,

enabling these small animals tomaintain condition on a high-

fibre diet through retention of microbes and potentially more

fermentable small particles for more complete digestion

(Hume et al. 1993; Pei et al. 2001). The present study did not

examine gut-passage of large particles and so no conclusion

can be drawn about the separation of digesta phases in the

swampwallaby, although based on comparative gut structure,

phase separation would be expected to be intermediate to the

large kangaroos and the smaller wallabies and potoroids.

Therefore, based on the small particle gut-retention time

recorded in the present study, large particle gut-retention

times of around 41 hr (31 hr spore MRT plus expected 10 hr

mean delay to large particle excretion) might be expected in

the studied swamp wallabies. Spores attached to sporocarp

fragments may pass through the gut with the large particle

phase (Comport & Hume 1998), resulting in spore gut-

retention times longer than for unattached spores. While the

extent to which swamp wallabies orally process sporocarps

prior to swallowing is not known, it is possible that naturally

ingested, whole sporocarps are not masticated and are

swallowed as fragments rather than as slurry. Because

wallabies in the present study were fed spores in a slurry,

estimates of spore gut-retention time in the studied wallabies

are considered conservative.

Manymammals are able to adapt to varying diet quality by

increasing gut capacity in response to more fibrous (lower

quality) diet, slowing the rate of passage of digesta to enhance

digestive efficiency, including bandicoots (Moyle et al. 1995)

and murid rodents (Gross et al. 1985; Hammond & Wunder

1991; Lee & Houston 1993). Rodents are also known to vary

gut capacity in response to changes in food intake (Hammond

&Wunder 1991). Similar responses to diet variation have been

observed in macropodids. In tammar wallabies the length of

the intestine and caecum (hindgut) increases in response to

a more fibrous diet, possibly to make secondary fermentation

in the hindgut feasible (Lentle et al. 2004). Osawa & Woodall

(1990) found that in swamp wallabies the length of the intes-

tinal villi increased, and therefore small intestinal surface

area increased relative to intestine size, with seasonal

increases in dietary fibre intake. The swamp wallabies in the

present study may have been consuming a higher-fibre diet

than usual, or higher-fibre relative to other browsing

wallabies, and concomitant changes in small intestine

morphology could have resulted in the longer than expected

gut-retention times observed. Further information on swamp

wallaby digestive anatomy and physiology, and changes with

diet, would be valuable in assessing the time taken for mac-

rofungal spores to pass through the gut of the swampwallaby.

The gut-retention times observed in swampwallabies in the

present study could also be due to different methodology,

including activity level, diet quality, feed intake and particle

size, compared to other studies. In the present study, animals

were able to select from food items including native grasses,

browse, macrofungal sporocarps and supplementary feeds

(lucerne hay, pelleted feed and apple), while in most studies

animals were fed experimental diets consisting primarily of

pelleted feed. Pelleted or milled feed can reduce particle and

fluid gut-retention times in sheep (Fadlalla et al. 1987) and

wallaroos (Freudenberger&Hume1992) because particle size at

ingestion is already sufficiently small for digestion. Although I

didnotassessuptakeof thesupplementary feedoffered relative

to natural food items in the present study, little supplementary

feed appeared to be taken and so the requirement for masti-

cation of natural food items may have contributed to a longer

digestion time. Conversely, the marker spores were fed in

a slurry ofmacrofungal sporocarp to the back of themouth and

would not have required mastication. Possibly, the sporocarp

slurry did not begin to pass through the gut until a subsequent

bout of feeding brought in other digesta.

Mycophagous vs non-mycophagous macropodoidmarsupials

Macropodoid species known to consume sporocarps (whether

stronglymycophagousornot), and forwhichgut-retentiondata

were available, retained fluid and small particles longer in the

gut than non-mycophagousmacropodoids, although statistical

support for this effect was weak. A larger sample size would

help clarify this comparison. Differences in gut-retention time

might reflect the different body size, diet quality and gut

Fig 2 e (A) Proportion of marker spores excreted by swamp

wallabies after oral dosing. (B) Cumulative proportion of

marker spores excreted by swamp wallabies after oral

dosing. Circles[ 21 kg male, triangles[ 10 kg male.

206 M.A. Danks

Author's personal copy

morphology ofmycophagousmacropodoids. Species known to

bemycophagous tend to be smaller, consume less fibrous diets

and have a sacciform forestomach-dominated gut structure, as

compared to non-mycophagous macropodoids which tend to

be larger, have a specialised grazing (fibrous) diet, and a tubi-

form forestomach-dominated gut structure (Freudenberger

et al. 1989). These features of mycophagous macropodoid

anatomy and feeding strategy enable utilisation of putative

low-quality food items such as macrofungal sporocarps. Addi-

tionally, these species occur predominantly in the mesic

eucalypt-dominated (EM) forests andwoodlands of Australia in

whichEMsporocarps, particularly truffle-like fungi, areahighly

diverse and abundant food resource (Claridge & May 1994;

Johnson 1994a; Allen et al. 1995; Bougher 1995; Claridge et al.

2000; Bougher & Lebel 2001). A diversity of fungi is probably

important for a balanced fungal diet (Claridge & Trappe 2005).

Macrofungal sporocarps have been considered a low-

quality food item because much of the nutrient content is in

indigestible forms or associated with cell walls (Cork & Foley

1990) requiring special gut adaptations, such as microbial

fermentation, for nutrient absorption. However, foregut

fermentation, as compared to hindgut fermentation, is

thought to improve the nutritional value of fungal sporocarps

for mammals by enabling better digestion of complex amino

acids through microbial fermentation in the forestomach

(Kinnear et al. 1979; Claridge&Cork 1994; Johnson 1994b). Most

foregut fermenting potoroids rely heavily on sporocarps, and

some macropodids, including wallabies and pademelons,

consistently consume sporocarps as part of amore varied diet.

The swamp wallaby, as a foregut fermenter, probably derives

nutrition from macrofungal sporocarps to supplement the

plant browse component of its diet, and retaining sporocarp

digesta in the gut for longer may enhance absorption of

nutrients from this relatively indigestible food item.

Spore gut-passage in other mycophagous mammals

Hindgut fermentingmammals also regularly utilise fungi, and

some, such as the northern flying squirrel (Glaucomys sabrinus)

(Maser et al. 1985; Vernes et al. 2004), rely heavily on macro-

fungal sporocarps, despite their apparently limited ability to

digest the ‘unavailable’ nutrients in these foods (Cork &

Kenagy 1989a; Bozinovic & Mu~noz-Pedreros 1995; D’Alva

et al. 2007). Among the Australian hindgut fermenters, all

weighing less than 3 kg, some (e.g. bush rat, Tory et al. 1997)

rely seasonally upon sporocarps and many, including other

rodents, peramelids and possums, consume sporocarps

regularly or occasionally (Claridge & May 1994; Claridge et al.

1996). Some of these animals have long gut-retention times,

for example the common brushtail possum and the giant

white-tailed rat. The giant white-tailed rat retains large

particulate digesta in an enlarged fundic diverticulum, slow-

ing the rate of passage of particulate digesta and increasing

absorption of nutrients (Comport & Hume 1998). Physiological

and morphological adaptations of the hindgut such as these

improve hindgut fermentation capabilities and consequently

enhance utilisation of otherwise low-quality food items such

as macrofungal sporocarps (Claridge et al. 1999).

Mycophagous mammals perform an important spore

dispersal role particularly for truffle-like fungi, which rely

upon such vectors for longer-distance spore dispersal.

Weighted average of available fluid and particle gut-retention

time estimates for mycophagous mammal species sympatric

with the swamp wallaby range from 12 hr (red-necked pade-

melon), to more than 2 d (brushtail possum). A community of

mammals with varying foraging habits, microhabitat use

patterns, home range size, and gut-retention times would

result in dispersal of spores of the truffle-like sporocarp

community to a variety of microhabitats and distances from

points of ingestion. Spore dispersal at multiple scales is likely

to be vital in maintaining macrofungal community diversity,

populations and individuals.

Mean gut-retention time of macrofungal spores alone does

not characterise an animal’s spore dispersal role but it is

a useful measure of the time after ingestion at which most

ingested spores are deposited in faeces; so it is a useful metric

when assessing spore dispersal by mycophagous mammals.

Variance in gut-retention time may also influence spore

dispersal patterns. Combining information on spore retention

with movement patterns, distance travelled, or area covered

within the average gut-retention time is also important, and

would enable relative rates of macrofungal spore dispersal by

mycophagous mammals to be examined. Further studies of

spore gut-passage in wild swamp wallabies and other

mycophagous mammals under semi-natural conditions are

necessary to obtain statistically robust and ecologically

meaningful measures of spore gut-retention time. Additional

information on the diversity and amounts of sporocarps

eaten, defecation patterns, and the viability of spores on

passage through the gut of mycophagous mammals with

varying digestive physiology would also be valuable in

building a picture of spore dispersal within a community of

mycophagous mammals.

Acknowledgements

This work was funded by a Hermon Slade Foundation grant

(HSF08-6, to K. Vernes, T. Lebel, and the author) and an Austra-

lian Research Council Discovery Grant (DP0557022) to K. Vernes.

TheauthorwassupportedbyanAustralianPostgraduateAward.

Research was conducted under University of New England

Animal Ethics Committee approval (AEC09-023), andNewSouth

Wales National Parks and Wildlife Service scientific license

(S12493). University of New England provided facilities and

access to Newholme Field Station. I thank S. Steinhart for

assistance inthefield,andK.Vernes,T. Lebel,N.Andrew, J. Price,

and three anonymous reviewers for critical feedback and

constructive comments that greatly improved this manuscript.

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