A survey of frog odorous secretions, their possible functions and phylogenetic significance

Abstract

This study provides a survey of frog odour (with particular reference to Australian species) and discusses the human perception and classification of frog volatile secretions. Professional and amateur herpetologists were solicited for information on the frogs they perceived as odorous. In addition, volunteers were asked to smell stressed frogs and describe the odour that they perceived. A total of 131 species, representing 30 genera (14 Australian and 16 other) and 11 families were assessed for odour. Odours ranged from pleasant floral aromas (e. g. Notaden spp. and Neobatrachus spp.) through to acrid, repulsive odours (e. g. Litoria alboguttata). The systematic relationships of these odours and their potential biological roles are discussed.

Full text

A survey of frog odorous secretions, their possible functions
and phylogenetic significance
Benjamin P.C. Smith1,2, Craig R. Williams3, Michael J. Tyler1, Brian D. Williams1
1School of Earth and Environmental Sciences, The University of Adelaide, SA 5005, Australia
2ChemComm Enterprises,163 route du Léman, 74160 Archamps, France
Corresponding author; e-mail: geocrinia101@yahoo.com.au
3School of Pharmacy and Biomedical Sciences, University of South Australia, SA 5000, Australia
Present address: School of Public Health and Tropical Medicine, James Cook University, Qld 4870,
Australia
Abstract. This study provides a survey of frog odour (with particular reference to Australian species)
and discusses the human perception and classification of frog volatile secretions. Professional and
amateur herpetologists were solicited for information on the frogs they perceived as odorous. In
addition, volunteers were asked to smell stressed frogs and describe the odour that they perceived.
A total of 131 species, representing 30 genera (14 Australian and 16 other) and 11 families were
assessed for odour. Odours ranged from pleasant floral aromas (e.g. Notaden spp. and Neobatrachus
spp.) through to acrid, repulsive odours (e.g. Litoria alboguttata). The systematic relationships of
these odours and their potential biological roles are discussed.
Key words: Frog; functional significance; odorous secretions; phylogenetic relationships; skin
secretions; volatile secretions.
Introduction
The integumentary glands of frogs produce a diverse range of chemicals. Com-
pounds isolated from frog secretions include bioactive peptides and proteins, guani-
dine derivatives, biogenic amines (e.g. dopamine and serotonin), steroids and al-
kaloids (for detailed reviews see Habermehl, 1981; Daly et al., 1987; Bevins and
Zasloff, 1990; Daly et al., 1993; Erspamer, 1994; Toledo and Jared, 1995; Daly,
1995, 1998a,b). In addition to these non-volatile components many frog species
emit volatile compounds (Smith, 2001) and a large proportion of these volatiles are
odorous (Brodie and Formanowicz, 1981; Tyler, 1976; Williams et al., 2000; Smith,
2001; Smith et al., 2003). For example, Noble (1931) noted that the secretions of
Rana septentrionalis (the aptly named “Mink Frog”) and Gastrotheca monticola
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48 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
(the Marsupial Frog) both smell like mink (Mustela vison, a small, semi-aquatic
weasel-like carnivore), and the European toad, Bufo vulgaris smells like vanilla.
Boulenger (1911) reports that some pelobatids smell like onions, Martin and Little-
john (1966) state that Litoria jervisiensis (Jervis Bay Tree-frog) smells like curry,
Tyler (1968, 1976) described the odour of L. infrafrenata (Giant Tree-frog) from
New Britain and L. aurea (Green and Golden Bell Frog) from New South Wales as
similar to that of dried thyme, Myers et al. (1991) commented on the defensively
malodorous, mercaptan-like odour of Aromobates nocturnes and Waye and Shew-
chuk (1995) noted that the skin secretion of Scaphiopus intermontanus (Great Basin
Spadefoot) smells like peanuts.
Despite interest in the chemistry of frog skin secretions, along with the fact
that numerous researchers and amateur naturalists have commented on the distinct
smell of many species of frogs and toads, there are few published records on
the analysis of anuran volatile chemicals or odorous secretions. The purpose of
this paper is to provide a comprehensive review of frog odours (as perceived by
humans) and hopefully stimulate research into the role and chemical identity of
volatile secretions. Particular reference is given to Australian species with data
drawn from literature searches, surveys, field observations and human sensory
studies.
In addition to the review, the question of whether the grouping of frogs by
‘odour similarity’ provides information about the phylogenetic relationship or
life history traits of the animals under study is considered. There is a need for
greater understanding of the compositions and properties of odours generally, quite
apart from their likely behavioural, pharmacological or ecological significance.
Comparative studies of frog odour may provide information about whether any
odours are common to all frogs, and whether any are species specific.
Amphibians are amongst the oldest terrestrial vertebrate animals on earth. They
originated from aquatic Devonian animals some 300 million years ago. Thus, the
taxonomic distribution of many of the compounds isolated from frog granular
glands corresponds to the classification based on other criteria (e.g. morphological
characteristics) (Cei and Erspamer, 1966; Roseghini et al., 1976; Erspamer et al.,
1984). Some groups of anurans (e.g. phyllomedusine and pelodryadine hylids)
contain large amounts of unique polypeptides, and each species has its own
characteristic polypeptide spectrum (Cei, 1963; Steinborner et al., 1996). The
dendrobatids are well known for their strong toxins; Phyllobates secrete mainly
batrachotoxins, which are highly toxic steroidal alkaloids, whereas Dendrobates
secretes a wide variety of less toxic and chemically simpler piperidine alkaloids
(Myers et al., 1978; Daly et al., 1987). Thus the biochemical differences in the
genera of dendrobatid frogs seem to have phylogenetic significance. Analyses of
biogenic amines (Cei et al., 1967, 1968, 1972) and secretions of the parotoid
glands (Low, 1972) of Bufo from throughout the world showed that trends in
these biochemical traits correspond to morphological groups of toads presumably
representing different evolutionary lineages. As odours are a result of the volatile

Frog odorous secretions 49
chemicals present in the skin glands, Williams and Tyler (1997) proposed that they
could be used to support relationships between taxa, and noted that the odours of
some Australian frogs related to species groups (as defined by Tyler and Davies,
1978). Furthermore, they suggested that odour could aid in field identification,
especially since morphologically similar species may differ greatly in odour (e.g.
Martin and Littlejohn, 1966).
Lastly, the potential role(s) of odorous secretions are discussed, both from a hu-
man and frog perspective. We are now aware of a vast array of secretions that
have antiviral, antifungal and antibacterial activity, together with others that are po-
tent analgesics or repel mosquitoes, rats or birds (Tyler and Smith, 2001). Odor-
ants secreted by frogs are an untapped source of bioactive compounds and un-
derstanding the effect these compounds have on humans and the role they play
in the frogs’ biology may lead to more novel amphibian-derived pharmaceuti-
cals.
As a major function of odour is the control of approach and avoidance behaviour
(Ehrlichman and Bastone, 1992), particular attention focuses on the defensive role
of odours in frogs. The idea that odorous/volatile compounds are defensive is
supported by reports that the vapour of some secretions will cause sneezing, nasal
discharge or congestion, or other generally irritating effects in humans (Minton,
1974; Nussbaum et al., 1983; Daly et al., 1987; Stebbins and Cohen, 1995; Smith,
2001; Smith et al., 2003). Furthermore, the olfactory and gustatory perception
of humans often have, in the past, suggested chemically protected organisms
(Wassersug, 1971; Brodie, 1983; Weldon and Rappole, 1997). Indeed, humans are
natural predators for some species and may be appropriate subjects in chemical
defence studies.
Aside from defence, odours may also play a role in pheromonal communication
(e.g. alarm pheromones, kinship recognition) or signify information about the
physiology of the frog (e.g. sex and breeding condition, health status) (Albone and
Shirely, 1984; Duvall et al., 1986; Albone and Natynczuk, 1992). For instance male
Rana muscosa have been observed to produce strong garlic-like odours during the
breeding season (Daerr, 2002).
Materials and methods
Information was obtained from both professional and amateur herpetologists re-
garding the frogs they consider odorous. Individuals on the membership lists of the
Australian Society for Herpetologists (ASH) and the Society for the Study of Am-
phibians and Reptiles (SSAR) were contacted. In addition, questions were posted on
the ASH mailing list (ash-l@mailbox.gu.edu.au), the USENET group sci.bio.herp,
and e-mail distribution list HERP-L (herp-l@ucdavis.edu). Amateur herpetologists
were targeted through the USENET group rec.pets.herp. In order to control for
odours arising from unnatural diets or as artefacts of captivity, respondees were also
asked about the status of the animals. Status descriptions included: field assessed

50 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
(F), short-term captive (<1 month) (SC), long-term captive (>3 months) (LC) and
laboratory bred (B).
Olfactory studies on the odours produced by Australian frogs were also con-
ducted. Where possible, odours were assessed from both field and captive frogs.
Unless specified, a minimum of four frogs were tested for each species. Where frogs
are listed as producing no odour, attempts were made to sample as many frogs as
possible. Most frogs were tested at a later date (>3 months after first presentation)
to eliminate seasonal variability and to the possibility of intermittent odour release.
Individuals of some species have been observed to produce odour during a stress
event followed by no odour in subsequent tests or initially produce no odour and
then release an odour when re-tested.
Naive volunteers (i.e. volunteers with no prior exposure to frog odour) were asked
to smell the secretion released by a stressed frog and describe, in five words or less,
the odour that they perceived. In addition, volunteers were asked whether they liked
or disliked the odour (i.e. the hedonic nature of the odour) and if it resulted in any
sensory sensation (e.g. tingling of the nose, headache, etc.).
Most frogs on handling or gentle prodding with forceps (Brodie, 1977) read-
ily emitted odorous secretions. If handling failed to release an odour mild elec-
trical stimulation of the skin muscles surrounding the glands was used to ex-
pel their contents (Tyler et al., 1992). All frogs were held by experienced han-
dlers and presented to the volunteers once the animal began secreting. Handlers
wore latex gloves to avoid contamination with human odour and prevent con-
tact with the secretion. Immediately prior to exposure volunteers were asked
to smell the latex gloves for one minute to familiarise themselves with that
odour.
Animals were held approximately 15 cm below the volunteer’s nose and the
volunteer instructed to breathe normally. If after five seconds no odour was
perceived the subject was asked to inhale deeply through their nose and to repeat
this procedure three times or until an odour was perceived. After three attempts, if
no odour was recognised, the stressed animals were removed.
Most observations were made with a minimum of eight volunteers. Where
possible, all volunteers were presented with at least four different animals to allow
for variation in odour descriptions. Initial presentations were at 5 minute intervals,
however, the volunteers were also given the opportunity to compare the odours of
the frogs at the same time. Volunteers were presented with pairs of frogs and asked
to score the ‘likeness’ of the odours on a scale of 1-9; 1 being dissimilar and 9
similar. If available, the same volunteers were tested one month later to determine
if any changes in odour were perceived. Prior to inclusion in the study the fitness
and health status of all volunteers was assessed against criteria formulated by the
University of Adelaide’s Human Research Ethics Committee. Following exposure
to the volatile secretion all subjects were monitored for half an hour to ensure that
no adverse reactions to the secretions occurred.

Frog odorous secretions 51
Results and discussion
From both the survey and olfactory studies a total of 131 species, representing
30 genera (14 Australian and 16 other) and 11 families were recorded (table 1).
Among the Australian frogs the proportion of odorous species in each family was
approximately the same (28 out of 41 hylids and 24 out of 41 myobatrachids
releasing odours). Differences, however, were obvious between genera. Of the two
hylid genera, the tree-frogs (Litoria) contained the greatest number of odorous
species (27 out of 33). The six species recorded as odourless (L. bicolor,L. ge-
nimaculata,L. inermis,L. meiriana,L. pallida and L. wotjulumensis) were studied
by Williams et al. (2000). The absence of odours for these frogs can neither be
confirmed nor refuted by this study, as specimens were unavailable for comparison.
Of the eight Cyclorana species only one was found to be odorous (C. platycephala).
Among the myobatrachids, odours were observed in the following genera:
Geocrinia (although Williams et al., 2000 recorded no odour), Heleioporus (R. Da-
vis, University of Western Australia states that Heleioporus spp. have weak, yet
characteristic and unpleasant odours; Williams et al., 2000, however, record no
odour for the two species they tested), Limnodynastes (3 of 7 species), Neobatra-
chus,Notaden,Pseudophryne and Uperoleia.Crinia,Paracrinia,Megistolotis and
Mixophyes all lacked odours. Odours for the last four genera cannot be ruled out,
however, due to the small number of species or individuals of each species assessed.
Although few Limnodynastes species produced odours, it has been reported that
most release secretions that stimulate the nasal mucosa, resulting in a warm, dry
sensation (pers. comm. G. Marantelli, Amphibian Research Centre, May 2001). Re-
assessment of all Limnodynastes species tested, using a select panel of five oenology
students instructed to record the hedonic nature of the secretions, confirmed this
observation for L. dumerilii,L. interioris,andL. terraereginae. These three species
all have tibial glands. The remaining species tested (all of which lack tibial glands)
did not appear to have the same sensory affect. However, the burnt odour produced
by L. peronii, and the burnt, fishy aroma released by L. fletcheri did, to some degree,
stimulate the nasal mucosa.
The majority of classifications obtained in this study are consistent with the work
by Williams and his colleagues (taking into account the variation in descriptive
terms used by volunteers). Five species of frogs previously described as having
no odour, however, were found by this study to release scents when stressed.
They were: Geocrinia laevis,Litoria gracilenta,Neobatrachus pictus,Notaden
melanoscaphus and Pseudophryne semimarmorata.
The greatest range of odours was observed in the hylid genus Litoria.Al-
though this may be an artefact of the greater number of species sampled com-
pared to other genera, the consistency of odours within other genera suggests other-
wise. With the exception of the sweeter, floral aromas of Neobatrachus and No-
taden, all odour-producing myobatrachids can be broadly grouped as producing
musty, earth-like odours. It should be noted that the earthy note described for the
myobatrachids, however, is distinct from that observed in the genus Litoria.In

52 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Table 1. Odour descriptions and hedonic assessment of the ‘defence’ secretions of Australian and foreign frog species obtained by surveying professional
and amateur herpetologists and by olfactory assessment using naive volunteers. The number in brackets following many of the descriptions indicates the
number of naive volunteers who used the term to describe the frogs’ odour. Captive status: F =Field assessed (i.e. odour characterised immediately following
collection); SC =Captured and held in captivity <1 month; LC =Captured and held in captivity >3 months; B =Bred. Source: OF(x, y ) =Olfactory
study (number of frogs used, number of volunteers); L =Literature; P =Personal communication (includes results from survey); PO =Personal observation.
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
Australian Frogs
Hylidae
Cyclorana australis
Giant Frog
No detectable odour F, LC L1 No observed effects Closely related to C. novaehol-
landiae.
C. australis species groupL2
C. cultripes
Knife-Footed Frog
No detectable odour LC OF(4, 8), L1,
PO
No observed effects Closely related to C. longipes,
C. maini,C. manya and
C. verrucosa.
C. brevipes species groupL2
C. longipes
Long-Footed Frog
No detectable odour FL1,SC
PO L1, PO No observed effects C. brevipes species groupL2
C. maini
Main’s Frog
No detectable odour LC OF(4, 8), PO No observed effects C. brevipes species groupL2
C. manya
Small Frog
No detectable odour F L1 C. brevipes species groupL2
C. novaehollandiae
New Holland Frog
No detectable odour SCOF, PO,LC
L1 OF(8,8), L1,
PO
No observed effects C. australis species groupL2
C. platycephala
Water-Holding
Frog
(A) Musty/muskyPO (1); Wet
burnt log (1); Characteristic but
difficult to describe (2).
(B) 25% dislike, 75% indiffe-
rent
FPO,SC
OF, PO OF(2,4), PO Slight irritation of nose Monotypic species group.
Possibly a separate genusP1,L2
C. verrucosa No detectable odour LC PO No observed effects C. brevipes species groupL2

Frog odorous secretions 53
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
Litoria adelaiden-
sis Slender Tree
Frog
Grass-like F L1 Monotypic species groupL3
L. alboguttata
Striped Burrowing
Frog
(A) Fresh, menthol, acridL1;
Acrid (1); Winter-green (1);
Spicy, acridP1, PO (3); Noxious,
foul (2); Faecal (1); Burnt euca-
lyptus leaves (1); Dry, spicy (1);
Heather absolute (1); Mossy,
spicy, green (2); Coumarin,
Hay-like (1). Similar to L. ran-
iformis but more earthy and
burntPO . (B) 100% dislike
FP1,SC
OF, PO,
LCL1
OF(3,14), L1,
P1, PO
Caused eyes to wa-
ter (lachrymation) and
severely irritated nasal
mucosa. Caused 1 vol-
unteer to gag
Genus enigmatic:
Closely related to C. australis
and C. novaehollandiae
(C. australis species group)L2.
Closely related to L. aurea,L.
dahlii, L. moorei and
L. raniformis (L. aurea species
group)L3
L. aurea Green and
Golden Bell Frog
Dried thymePO, L4;Acrid
L5;
DisagreeableL6 FL4, L5, L6,
SCPO
PO,L4,L5,L6 Caused eyes to sting
and water
L. aurea species groupL3
L. bicolor Northern
Dwarf Tree Frog
No detectable odour F L1 Closely related to L. fallax.
L. bicolor species groupL3
L. caerulea
Australian Green
Tree Frog
(A) Acrid, Bad, Distasteful,
Foul, Noxious, Offensive, Un-
pleasant (14); Asian food (2);
Biscuit (4); Boiled meat (1);
Bread (6); Butter (1); Buttered
popcorn (2); Corn chips (3);
Dirty socks (7); Earthy/Dusty
(2); Fungal (2); Grassy (1);
Hay (4); Herbs (1); Leaves
(1); Metallic (1); Musty (1);
NuttyL1 (77) - Almonds (2) -
‘Burnt’ (7) - CashewP1 (5) -
FL1, P1, P2, PO,
SCOF,
LCOF,L1,P1,P2,PO
,
BOF,L1,P2,PO
OF(20,148)
L1, P1, P2, PO
Non-volatile secretion:
- Accidental contact
with eyes caused acute
pain, stinging sensation
and watering.
- Contact with skin
resulted in erythema
and itchiness.
Volatile secretion:
- Resulted in headaches
and slight nausea on
prolonged exposure
Closely related to L. splendida.
L. caerulea species groupL3

54 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
PeanutsP2, PO (16) - Pine nuts
(1) - Walnut (1) - General (45);
Peanut brittle (1); Peanut butter
(3); Rice plants (1); Satay (3);
Savoury (3); Sesame oil (1);
Shellfish (cooked) (2); Sper-
mous (1); Urine (1); Woody (1);
Yeast (1).
Similar to L. splendidaP1, PO.
(B) 26% dislike, 74% indiffer-
ent/pleasant
L. chloris
Red-Eyed Tree
Frog
(A) Grass-likeL1; No odour (3
×bred juveniles)PO, P4;Un-
pleasant, strong spicePO (1);
Spicy curry (1); Dry, acrid,
spice (1); Mace-like (1); Foul,
Revolting, UnpleasantP3 (2).
(B) 100% dislike
SCOF, PO, P3,
LCL1,
BPO, P3, P4
OF(10,6), L1,
P3, P4, PO
Caused lachrymation
and severe irritation of
nasal mucosa.
Caused nauseous
feelingin3people
tested.
Closely related to L. gracilenta.
L. aruensis species groupL3.
Originally included in L. in-
frafrenata species groupL4
L. citropa
Blue Mountains
Tree Frog
(A) No odour (3 ×bred
juveniles)PO; Strong, distinct
(1); Unique (1); Penetrating (1);
Green,citrus,musky
PO, P2 (2).
Similar to L. spenceriP2.
(B) 20% like; 80% indifferent
FP1,SC
OF, PO,
BOF, PO, P2
OF(3, 5), PO,
P2
No observed effects Closely related to L. subglan-
dulosa,L. phyllochroa and L.
daviesae.
L. citropa species groupL3
L. dahli
Dahl’s Aquatic
Frog
(A) Sweet (‘sugary’), vegeta-
blePO; Sweet (2); Sweet, sharp,
alcoholic (2); Sweet mulch,
fresh wet leaves (4).
LC OF(4, 8), PO No observed effects L. aurea species groupL3

Frog odorous secretions 55
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
Slight similarity to L. rani-
formisPO.
(B) 100% indifferent
L. dentata
Bleating Tree Frog
Similar to L. ewingi but less
spicy and with a slight citrus
notePO.
Similar to L. ewingiP2
LC, B PO, P2 No observed effects Closely related to L. rubella.
L. rubella species groupL3
closely related to L. ewingiP1, P2
L. electrica (A) Grass-like, sourL1, PO;
Acrid, grass-like (1)P1 ; Grass,
dirt (2); Peat moss, Plant (1);
Wet rainforest (1); Earthy,
fungal (1); Eucalypt, earthy
(1); Damp carpet (1); Damp
clothes, mildewy (1); Rising
damp, musty (1); Adelaide tap
water, chlorine (1); Chemical
(1); Boccochini (Italian cheese)
(1). Similar to L. rubella and
L. ewingiP1, P2, PO. (B) 8% like;
62% dislike; 30% indifferent
FL1, P1,
SCOF, P1, PO
OF(3, 13), L1,
P1, PO
Stimulation of nasal
mucosa. Response to
the sensation varied
with most noting low to
no irritation. Three vol-
unteers, however, noted
a strong ‘chemical’
irritation
Closely related to L. rubellaP1
L. ewingi
Brown Tree Frog
(A) Grass-likeL1, P1 (6); Mown
lawn (2); Green vegetable (2);
Brussell sprout (1); Plant-like
(6); Potting soil (5); Earthy (1);
Earthy, grass (4); Earthy, mossy
(1); Mossy, green (1); Green
pea (3); ‘Light’, green (1); Her-
baceous, green (6); Spicy, green
FL1, P1, PO,
SCOF, P1, PO,
LCOF, P1, PO,
BOF, PO
L1, OF(37, 49),
P1, PO
Stimulation of nasal
mucosa, however, no
adverse perception.
Sensation ranged from
a sharp, fresh feeling to
a dry irritation con-
cordant with the
supplied ‘spicy/
Closely related to L. jervisiensis
and L. paraewingi.
L. ewingi species groupL3

56 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
(3); Peppery (1); Camphora-
ceous (1); Eucalypt, green,
earthy (1); Leaf litter, com-
posty, forest floor (3); Wet soil
with hint of ‘electrical fire’,
burning plastic (1). Distinct
variation in odours of individ-
ual frogs similar to L. rubella,
L. electricaP1, PO and L. den-
tataP2, PO.
(B) 100% indifferent
herbaceous’ description
L. fallax Eastern
Dwarf Tree Frog
MulchPO, P4 LC,B PO,P4 L. bicolor species groupL3
L. genimaculata No detectable odour LC L1 L. eucnemis species groupL3
L. gracilenta
Dainty Tree Frog
(A) No detectable odourL1 ;
Smoky, greenPO; Spicy (1),
Herbaceous (3); Green, curry
(1).
(B) 40% like; 60% indifferent
SCOF, PO,
LCL1, OF, PO
L1, OF(5, 5)
PO
Low-mild irritation of
nasal mucosa
L. aruensis species groupL3
L. inermis Peter’s
Frog
No detectable odourL1 FL1 L. latopalmata species groupL3
L. infrafrenata
Giant (or White-
Lipped) Tree Frog
Musky, spiceP5;Dried
thymeL4; CurryL1, P1, P2, PO FL4, P1, P2,
SCP5, PO,B
L1
L1, L4, P1, P2,
P5, PO
Relatively close relationship to
L. chlorisP1.
L. infrafrenata species group
L. jervisiensis
Jervis Bay Tree
Frog
CurryP6, P7, P8, L7;Musky
L8, PO F, LCPO P6, P7, P8 PO,
L7, L8
Low-mild irritation of
nasal mucosa
L. ewingi species groupL3.
Very closely related to L. little-
johni (species pair)P1

Frog odorous secretions 57
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
L. lesueuri
Lesueur’s Frog
Faintly grass-likeL1, PO FL1,SC
PO L1, PO Monotypic species groupL3
L. littlejohni
Heath Frog
Curry FP6, P8 P6, P8 L. ewingi species groupP1 .
Species pair with L. jervisien-
sisP1
L. meiriana
Rockhole Frog
No detectable odour LC L1 Monotypic species groupL3
L. moorei More’s
Frog
Characteristic, unpleasantP9 ;
Fresh, menthol, AcridL1 FL1,P9 L. aurea species groupL3
L. nasuta Rocket
Frog
Faintly grass-like F L1 L. freycineti species groupL3
L. pallida Pale Frog No detectable odour F L1 L. latopalmata species
groupL3A
L. paraewingi
Victorian Frog
(A) Grass-likeOF, similar to
L. ewingiP2, PO.
(B) 100% like
FP2, PO,SC
OF,
BPO
OF(1, 3), P2,
PO
Sharp, pleasant sensa-
tion
L. ewingi species groupL3.Very
closely related to L. ewingi.
The two species breed and pro-
duce hybrids in their narrow
zone of contact in north-eastern
VictoriaL9
L. peronii
Péron’s Tree Frog
(A) Sharp, plant-, grass-like,
spicyP10; Foul, Unpleasant (6);
Grass-like (1); Herb (3); Spicy,
green (1); Camphoraceous (2);
Peppery (2); Musty/mus-
kyP2, PO (10); Musty, wet
hair-likeL1. Distinct variation
amongst individualsP2, P9, PO.
(B) 72% dislike; 28% indiffer-
ent
FOF, P2, P10, PO,
LCL1, PO
L1, OF(6, 25),
P2, P10
Mild – strong irritation
of nasal mucosa
Closely related to L. rothii
(L. peronii species group)L3

58 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
L. phyllochroa
Leaf-Green Tree
Frog
(A) Green, cheesy (1);
Sweet, sweaty foot (3); Fatty,
greenPO. Similar, but sharper
than L. citropaPO. (B) 50% dis-
like; 50% indifferent
SC OF(2, 4), PO Pleasant sensation L. citropa species groupL3
L. raniformis
Southern Bell Frog
(A) Faecal (2); MossyP10;
Earthy (1); Fresh, menthol,
acridL1; Menthol (1); Green,
earthy (1); Wet grass and
soilPO (1); Fresh (1); Raw
mushroom (2); Fungal, mould
(1); Unpleasant (1); Sharp,
fungal (1); Coumarin, hay-like
note (1); Forest floor, damp (2);
Cut grass (1); Benzene-like (1);
Kiwi fruit and pear lollies (1);
GarlicP11. (B) 28% like; 33%
dislike; 39% indifferent
FP9, P10, PO,
SCOF, PO
L1, OF(4, 18),
P10, P11, PO
Sensation ranged from
a fresh feeling to mild
irritation of the nasal
mucosa (not unpleas-
ant)
L. aurea species groupL3
L. rothii
Roth’s Tree Frog
(A) Mild fishL1;Rawred
meat (1); Rotting meatP1 (3);
Earthy, metallic, fungal (1);
Dank, swampy (2); Rotten eggs
(2); Sulphur; Hydrogen Sul-
phide, Sodium sulphite (4);
Vinegar (1); Weird (1); Potent
(1); Foul (3); Mud, wet, damp
(1); Rotten leaves (1); Sweet,
rotting smellPO; Plant, creek
smell (1); Hard to describe but
not unpleasant (1). (B) 87% dis-
like; 13% indifferent
FP1, PO,SC
OF,
LCL1
L1, OF(12, 23),
P1, PO
Induced feelings of
nausea in some volun-
teers but did not appear
to irritate
L. peronii species groupL3

Frog odorous secretions 59
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
L. rubella
Red (or Desert)
Tree Frog
(A) Grass-like, sour, acrid at
timesL1; Sharp, grass-like (1);
Plant-like (3); Broad beans,
peppermint (1); Garden/nursery
smell (4); Potting soil (3);
Earthy, wet peat mossPO (1);
Detergent, chlorine (1); Rain-
forest, rotting logs, ferns and
pine trees (1); Fungal, earthy
(1); ‘cool’ (1); ‘warm’, used
sneakers (1); Pine, grass, saw-
dust (1); Hardware product
‘Selley’s all clear’ (1). Distinct
variation in odours from differ-
ent geographic locations. Simi-
lar to L. electrica and
L. ewingiPO. (B) 5% dislike;
95% indifferent
FL1, PO,
SCOF, PO
L1, OF(15, 20),
PO
Mild irritation of nasal
mucosa
L. rubella species groupL3
Closely related to L. electricaP1
L. spenceri
Spotted Tree Frog
Fresh, Sharp, Faint PinePO;
DisinfectantP2; AntisepticP3 LC,B P2,P3,PO
L. splendida
Magnificent Tree
Frog
(A) NuttyL1, PO - Cashew (2)
- Peanut (6). Similar to L.
caeruleaL1, PO. (B) 100% like
SC, LC, B L1, OF(3, 8),
PO
L. caerulea species groupL3
L. subglandulosa
Glandular Frog
(A) Decomposing grass clip-
pings (1); Decomposing vege-
tation (1); Sweet, compost (1);
Green-leafPO (2). (B) 100% in-
different
LC OF(1, 5), PO L. citropa species groupL3

60 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
L. wotjulumensis
Wotjulum Frog
No detectable odourL1 F, LC L1 L. nigrofrenata species groupL3
Myobatrachidae
Crinia haswelli
Haswell’s Froglet
No detectable odour F, LC, B PO No observed effect
C. parinsignifera
Eastern Sign-
bearing Froglet
No detectable odour F, LC PO No observed effect
C. remota
Remote Froglet
No detectable odour L1 FL1
C. riparia Stream-
bank Froglet
No detectable odour L1, PO F, LC L1, PO No observed effect
C. signifera
Common Froglet
No detectable odour L1, PO F, SC, LC, B L1, PO No observed effect
Geocrinia laevis
Smooth Frog
No detectable odourL1;Musty,
wet dirtP10, PO. Similar to
Pseudophryne spp.PO
FP9,PO,B
L1, PO L1, P10, PO Low-mild irritation
Heleioporus spp. Characteristic odour F P9 Volatile secretion:
- LachrymationP9.
Non-volatile secretion:
- Lachrymation and in-
tense irritation/burning
sensation following ac-
cidental eye contactL10.
- Ingestion of secretion
resulted in dry, swollen
lips and mouth, tight-
ness of the respiratory

Frog odorous secretions 61
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
tract leading to restrict-
ed breathing and re-
duced heart rateL10, L11
H. australiacus Gi-
ant Burrowing Frog
No detectable odour F P8
H. eyrei
Moaning Frog
No detectable odour F L1
Limnodynastes spp. F, LC, B P2 All stimulate the nasal
mucosa-feeling warmth
L. convexiusculus
Marbled Frog
No detectable odourL1 LC L1
L. dumerilii Four-
Bob (or Eastern
Banjo) Frog
(A) Warm, dry sensation (7);
Musty, spicy, earth-like (1);
Warm, shirazPO. (B) 100% in-
different
F, LC OF(8,8), PO Dry/warm sensation.
Nonvolatile secretion
of tibial gland aversive
to ratsL11A
L. fletcheri
Marsh (or Long-
Thumbed) Frog
Musty, burnt, fishy F P10, PO No observed effect
L. interioris
Giant Banjo Frog
Dry/warm sensation (no real
odour)
LC PO Dry/warm sensation
L. peroni Brown-
Striped Frog
Musty, burnt F LI, OF(12,8),
P10, PO
No observed effect
L. tasmaniensis
Spotted Grass Frog
No detectable odour FL1, PO,SC
OF,
BPO
L1, OF(14,8),
PO
No observed effect
L. terraereginae
Northern Banjo
Frog
No detectable odour B PO Dry/warm sensation
Megistolotis lignar-
ius
Carpenter Frog
No detectable odour LC L1 Genetic studies suggest this
genus should be synonymised
with LimnodynastesP1

62 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
Mixophyes fascio-
latus Great Barred
Frog
No detectable odour LC, B (juve-
nile)
PO No effect
M. schevilli North-
ern Barred Frog
No detectable odour F L1
Neobatrachus cen-
tralis Trilling Frog
(A) Fermented meat-likeL1, PO
(2); Sweet, red meat (1); Sweet,
unpleasantP10 (5). (B) 87.5%
dislike; 12.5% indifferent
FL1, P10, PO,
SCOF
L1, OF(5,8),
P10, PO
Nauseous sensatiom
N. pictus Painted
Frog
(A) No detectable
odourL1; Sweet, floral (4);
FloralP3, P10, PO (6); Toilet
freshenerP2 (2). (B) 100% like
FP10, PO,SC
OF,
LCL1,B
P2, P3
L1, OF(12,8),
P2, P3, P10,
PO
Fresh, pleasant sensa-
tion
N. sudelli Sudell’s
Frog
(A) Floral. (B) 100% like FP10, PO,SC
OF,
BP2, P3, PO
OF(5,8), P2,
P3, P10, PO
Pleasant sensation
Notaden bennetti
Crucifix (or Holy
Cross) Toad
(A) Sharp, sweet, floral.
(B) 100% like
SC OF(4,8) PO Pleasant sensation
N. melanoscaphus
Northern Spadefoot
Toa d
(A) No detectable odourL1 ;
FloralPO (4); Hand soap (1);
Colonge (1). (B) 100% indiffer-
ent
LC L1, OF(3,6),
PO
Pleasant, mild irritation
N. nichollsi Desert
Spadefoot Toad
No detectable odour LC L1
Paracrinia haswelli
Haswell’s frog
No detectable odour B L1
Pseudophryne spp. Musty, dirt-like F, LC, B P2
P. bibronii Bibron’s
Toa dlet
(A) Musty, earth-likePO;Wet
dirt (8). (B) 100% indifferent
FPO,SC
OF,
BPO
OF(4,8) PO Mild irritation, not un-
pleasant

Frog odorous secretions 63
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
P. coriacea Red-
backed Toadlet
Musty, wet dirt LC, B P2, P3, PO
P. corroboree
Corroboree Frog
(Toadlet)
Musty, wet dirt LC, B P2, P3, PO
P. dendyi Southern
Toa dlet
Musty, wet dirt LC, B P2, P3, PO
P. guentheri Gün-
ther’s Toadlet
Unpleasant. Not very pungent
or obvious
FP9
P. occidentalis
Wes tern (or
Orange-Crowned)
Toa dlet
Unpleasant. Not very pungent
or obvious
FP9
P. semimarmorata
Southern Toadlet
No detectable odourL1;Musty,
dirt-likeP2, PO FP2, PO,
LCP2, PO,
BL1, P2, PO
L1, P2, PO
Uperoleia altissima Musty, earth-like F L1
U. aspera
Derby Toadlet
Musty, earth-like LC L1
U. borealis
Northern Toadlet
Musty, earth-like LC L1
U. inundata Flood-
plain Toadlet
Musty, earth-like F L1
U. lithomoda
Stonemason
Toa dlet
Musty, earth-like F, LC L1
U. littlejohni Little-
john’s Toadlet
Musty, earth-like F, SC, B L1, PO

64 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
U. martini Martin’s
Toa dlet
No detectable odour LC PO
U. mjobergii
Mjöberg’s Toadlet
Musty, earth-like LC L1
U. talpa
Mole Toadlet
Musty, earth-like LC L1
Microhylidae
Cophixalus ornatus Musty, earth-like F L1
Ornate Frog
Other Frogs
Bufonidae
Bufo spp. (Yemen) Males — garlic and mint
(toothpaste like). Females —
no odour
FP11
B. boreas
Wes tern Toa d
Characteristic, spicy, similar to
R. pretiosa but not as bitterP13;
Peanut butter, similar to
B. punctatasP14
F P13, P14
B. marinus Marine
(or Cane) Toad
No detectable odourL1, PO;
Statement made in reference to
chemical defence that the cane
toad secretion smellsL12
LC, F L1, L12, PO Non-volatile secretion:
- Accidental contact of
secretion with
eye caused intense
painL10, P1, PO
B. punctatus
RedSpottedToad
Peanut butter F P14
B. viridis Malodorous, unpleasant P27

Frog odorous secretions 65
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
B. vulgaris
European Toad
Vanilla L13
B. spinulosus Malodorous P27
Discoglossidae
Alytes obstetricans
Midwife Toad
Characteristic smell. Statement
made that “the smell is so pow-
erful that it deters almost all
predators”
L14
Bombina bombina
Red Unk
Characteristic smell L15 Skin secretions cause
severe sneezing and
catarrh-like symptoms
in humansL15
Bombina orientalis Garlic PO Slight irritation of nasal
mucosa
B. variegata Yellow
unk
Characteristic smell L15 Skin secretions cause
severe sneezing and
catarrh-like symptoms
in humansL15
Hylidae
Gastrotheca monti-
cola
Mink L13
Phrynohyas venu-
losa Marbled Tree
Frog
Distinct odour P15
Hyla chrysoscelis Cooked, steamed green vegeta-
bles; Runner beans
P1, P16, PO
H. arenicolor
Canyon Tree Frog
Stinky P19

66 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
H. ebbracata Malodorous P19
H. regilla Characteristic odour, difficult to
describe
P15
H. versicolor Smell noted but not described L16 Secretion shown to
repel shrews/prevent
feedingL17
Osteopilus septen-
trionalis
Cuban Tree Frog
Sweet, cappuccino-like P19 Irritating to hands and
eyesP19
Phyllomedusa spp. Disagreeable L6
Phyllomedusa
rohdei
Strong odour L17
P. tomopterna
Tiger leg Monkey
Frog (or Lemur
Tree Frog)
Acrid rotting leaves L18
Dendrobatidae
Aromobates noctur-
nus
Unpleasant L19
Pipidae
Xenopus laevis
African clawed
toad
Indescribable yet distinct/
characteristic to the clawed
toadP17; No odour (8 frogs
tested)PO
FP17,B
PO P17, PO Inhibits feeding in
some snakesL20, L21
Pelobatidae
Pelobates sp. Onion L22

Frog odorous secretions 67
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
P. fu s cu s
Garlic Frog
GarlicL23, L24; DisagreeableL4 ;
MalodorousP27 L6, L23, L24,
P27
Scaphiopus spp. Disagreeable odourL6, L26;
PeanutsP18 L6, L25, P18 Irritation and watering
of the eyesL26
S. hammondii
Western spadefoot
toad
Roasted peanuts L27
S. intermontanus
Great Basin Spade-
foot
Peanut L28 Irritating to eyes (burn-
ing sensation when
accidentally rubbed in
eyes)
S. holbrookii Skunk P19
S. holbrookii
hurterii Hurter’s
Spadefoot
Disagreeable odour L29, L24
Pelodytidae
Pelodytes sp. Onion L22
Pelodytes punctatus
European Parsley
Frog
Parsley P20
Ranidae
Rana a. aurora
The Northern Red-
Legged Frog
Garlic (not consistent — some
frogs on handling don’t produce
any odour)
P21
Rana capito
Gopher Frog
Distinct odour P22 Irritating to eyes. Ex-
periments show the se-
cretiontobehighly
toxic (unpubl. data)P22

68 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
R. cascadae
Cascades Frog
Garlic (not consistent) P21
R. clamitans Mink-like L30
R. hechsheri
River Frog
MuskyP21 Tadpoles — peculiar,
sweetish odourL13 P21, L13
R. luteiventris
Columbia Spotted
Frog
Reminiscent of new plastic
products. Odour produced by
juveniles and adults of both
sexes. Not detected in meta-
morphs
P23
R. muscosa Moun-
tain Yellow-Legged
Frog
Garlic P21, L31
Rana palustris
Pickerel Frog
Alfalfa sprouts P19 Non-volatile secretion
observed to kill other
species of frog on
contactL32
Rana pretiosa Ore-
gon Spotted Frog
Distinct odour, Bitter, spicy –
similar to western toads
(B. boreas) but not as bitter
P13
Rana septentrion-
alis Mink Frog
MinkP24; Mink/AnimalisticPO;
FoulP25;Urine
P19;
DisagreeableL6
F L6, P19, P24,
P25, PO
Mantella au-
rantiaca Golden
Mantellid
Peppery LC P26

Frog odorous secretions 69
Table 1. (Continued).
Species Reported odours (A) and hedo-
nic assessment* (B)
Captive status Source Observed effects#Taxonomic relationships
Hyperoliidae
Phlyctimantis
verrucosus
Bad smelling L33
*Percentage like/dislike/indifference only relates to observations made during the olfactory analysis of Australian frogs. No attempt has been madeto
standardise results against number of volunteers.
#Observed effect of volatile secretions unless otherwise stated.
Personal reports: P1 =Mike Tyler (Adelaide University: mtyler@adelaide.edu.au); P2 =Gerry Marantelli (Amphibian Research Centre, Melbourne:
arc@frogs.org.au); P3 =Raelene Hobbs (Amphibian Research Centre); P4 =Russel Traher (Melbourne Zoo: russel.traher@zoo.org.au); P5 =Deb-
orah Pergolotti (Cairns Frog Hospital: frogcrusader@north.net.au); P6 =John Wombey (CSIRO, Wildlife and Ecology: John.Wombey@dwe.csiro.au);
P7 =David, Frog and Tadpole Study Group (david@fats.org.au); P8 =Frank Lemckert (Research and Development Division, State Forests of
NSW: frankl@sf.nsw.gov.au); P9 =Robert Davis (University of Western Australia: rdavis@upnaway.com); P10 =Steve Walker (EPA, South Aus-
tralia: sjwalker@visto.com); P11 =Peter Robertson (wildlife.profiles@bigpond.com); P12 =John Mulder (Mulder.J@net.HCC.nl); P13 =Jay Bow-
erman (bowerman@empnet.com); P14 =Terry Schwaner (Southern Utah University: Schwaner@suu.edu); P15 =Cal King (getulus@no bull.com);
P16 =Mark Hutchinson (South Australian Museum: hutchinson.mark@sagov.sa.gov.au); P17 =Jack Crayon (University of California, Riverside:
crayoj@student.ucr.edu); P18 =Renata Plattenberg (plattenberg@yahoo.com); P19 =Jackie Grant (Cornell University: jbw1@cornell.edu); P20 =Andy
Stevenson (andy.cc.stevenson@postoffice.co.uk); P21 =Sean Barry (University of California, Davis: sjbarry@ucdavis.edu); P22 =John Jensen (Georgia
DNR, Nongame-Endangered Wildlife Program: John_Jensen@mail.dnr.state.ga.us); P23 =Bryce Maxell (University of Montana: nathist@selway.umt.edu);
P24 =Bob Ling (Kankakee Community College: bling@kcc.cc.il.us); P25 =Mel (Herpfrog@aol.com); P26 =Edward Kowalski (Philadelphia Zo-
ological Society: EdwardK674@aol.com); P27 =Ulrich Sinsch (University of Koblenz-Landau: sinsch@uni-koblenz.de). Literature sources: L1 =
Williams et al. (2000); L2 =Maxson et al. (1985); L3 =Tyler and Davies (1978); L3A =Davies, Martin and Watson (1983); L4 =Tyler (1968);
L5 =Tyler (1976); L6 =Duellman and Trueb (1986); L7 =Martin and Littlejohn (1966); L8 =Cogger (2000); L9 =Dennington (1990); L10
=Tyler (1987); L11 =Softly and Nairn (1975); L11A =Crook and Tyler (1981); L12 =Stoddart (1980); L13 =Noble (1931); L14 =Wildlife
Fact-File card 3 (1997); L15 =Habermehl (1981); L16 =Brodie and Formanowicz (1981); L17 =Sazima (1974); L18 =Tigerleg Monkeyfrogs,
http://www.mascarino.com/VariousTiglerlegMonkeyfrogs.html (accessed 25th October 2000); L19 =Myers et al. (1991); L20 =Zielinski and Barthal-
mus (1989); L21 =Barthalmus and Zielinski (1988); L22 =Boulenger (1911); L23 =Mattison (1987); L24 =Lábler et al. (1968); L25 =Conant and
Collins (1991); L26 =Minton Jr. (1974); L27 =Stebbins (1985); L28 =Waye and Shewchuk (1995); L29 =McCoid et al. (1999); L30 =Minenesota
Herpetology, http/:www.earthvision.asu.edu/∼joe/Minnesota-Herpetology/frogs_toads/Green_frog (accessed 20th January 2003); L31 =Grant (2001); L32
=Oulahan (1976); L33 =Drewes and Vindum (1994).

70 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Litoria the earthy aroma is reminiscent of an organic loam/potting mix, whereas
the earthy note for the myobatrachids shows greater similarity to a wet clay soil.
Such generic classification highlights the difficulty in assigning odour classifica-
tions.
Intraspecific variation in odour was rare. The sampling of several individuals from
a single locality revealed little to no detectable variation in odour type. Notable
exceptions were the tree frogs, L. ewingi (see figure 1) and L. peronii. Geographical
variation in species odour was also minimal, the exceptions being L. ewingi,
L. peronii,L. rubella andtosomedegreeL. raniformis. The difference in L. rubella
odour was not wholly unexpected in the light of previous work documenting
conspicuous differences in the nature of skin peptides amongst different populations
(Steinborner et al., 1996). In addition, L. rubella includes allopatric populations
throughout northern Australia that differ slightly in morphology. However, because
of the small number of frogs sampled from each locality it was difficult to
characterise the differences in odour. All animals produced odours, which were
all variations on a similar theme (i.e. all smelled more or less grass-like) and
sour, despite some being detectably different (frogs were sampled from Farina
Station, Flinders Ranges, South Australia; Nutwood Downs Station, Northern
Territory; Gladstone, Queensland and Carrington Falls Quarry, Queensland). On
the other hand, while the peptide profiles of L. caerulea from different locations
are seen to differ (Donnellan et al., 2000), no obvious change in odour was
perceived for this species of frog with repeated observations over time (Smith et
al., 2003).
Odour differences for captive-bred frogs and those caught in the field were
observed for the following species: L. ewingi (see figure 2) and L. paraewingi
(slight difference). This variation suggests that environmental factors may play a
role. For instance, the presence of certain molecules in unrelated species may be
the result of their production not by the vertebrates themselves but from exogenous
environmental sources such as the diet — dietary uptake of toxins is well recognised
in frogs; classic examples being the uptake and retention of lipophilic alkaloids
secreted by the dendrobatid frogs of South America (e.g. Daly et al., 1994) and
cantharidin by Rana pipiens (Eisner et al., 1990) — or from indigenous skin-
surface microflora. For example, the presence of tetrodotoxin in the pufferfish Fugu
poecilonotus is produced by Pseudomonas spp. present on the skin surface of the
fish (Yotsu et al., 1987).
Chemical studies on the odour of L. ewingi support the role of environmental
factors in the odour of at least this species. Principle components of the frog’s
odour were identified as plant monoterpenes (Smith, 2001), the synthesis of
which are restricted to higher plants, microorganisms and a few marine and
terrestrial vertebrates (Banthorpe and Charlwood, 1972; Hanson, 1985; Erman,
1985; Charlwood and Banthorpe, 1991). Furthermore, GC-MS analysis showed that
the profile of both long-term captive (>12 months) and bred animals did not contain
terpenes and that the level of terpenes in the secretion of wild caught frogs decreased

Frog odorous secretions 71
Figure 1. Within group similarity of odours assessed using volunteers familiar with the odour of
Litoria ewingi secretions. Ten volunteers were presented with pairs of wild and captive frogs and asked
to score ‘likeness’ of the odours on a scale of 1-9; 1 being dissimilar and 9 similar. Data represent the
mean ‘likeness’ score. Error bars show standard deviation from the mean. A total of five frogs for each
group were assessed.
over time — a rapid decrease in the amount and composition of terpenes was seen
after 2-3 months (Smith, 2001).
Two explanations were proposed for the presence of terpenes in the skin secretion
of L. ewingi: dermal and/or dietary uptake. Due to the non-destructive nature of our

72 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
Figure 2. Similarity of wild caught Litoria ewingi from two distinct populations to captive raised
animals. Ten naive volunteers were presented with pairs of wild and captive frogs and asked to score
‘likeness’ of the odours on a scale of 1-9; 1 being dissimilar and 9 similar. Data represent the mean
‘likeness’ score. Error bars show standard deviation from the mean. A total of 30 frogs (10 from each
treatment) were used.
sampling technique (see Smith et al., 2000) we were able to detect changes in the
volatile profile of frogs fed terpene-dosed prey (dietary uptake) and frogs placed
in contact with foliage known to contain a high terpene content (Eucalyptus sp.)
(dermal uptake), over time (Smith, 2001).
Bred L. chloris and L. citropa from Melbourne Zoo lacked odours, however
bred individuals from the Amphibian Research Centre produced odours similar
to long term captive specimens. No difference was observed between bred and
field odours of Crinia signifera,Geocrinia laevis,Litoria caerulea,L. dentata,
L. fallax,L. infrafrenata,L. spenceri,L. splendida,Limnodynastes tasmaniensis,
Pseudophryne semimarmorata and Uperoleia littlejohni. Thus, it is unlikely that
environmental factors play a role in odour production for these species. Finally,
although a number of frogs have been classified as producing no odour, odours for
these species cannot unequivocally be ruled out as they may fall below the human
olfactory system’s odour threshold.
Most odours seemed to fit into discrete groups: nutty, ‘green’ (including grass-
like and herb-like), spice-like, earth-like or unpleasant (adapted from Williams and
Tyler, 1997; Williams et al., 2000). In some cases the frogs within these “odour
groups” reflect the species groups within the genus Litoria as suggested by Tyler
and Davies (1978). For example, L. caerulea and L. splendida (L. caerulea group)
smell of nuts, whereas L. infrafrenata (L. infrafrenata group), which is also large
and green, smells of curry. The L. infrafrenata reported here came from northern
Queensland, whereas the specimen reported by Tyler (1968) (which smelled like
dried thyme) was from New Britain. The odours of the two populations are quite
different, providing support for morphological data indicating that the population
status of subspecies (L. infrafrenata infrafrenata and L. infrafrenata militaria) could

Frog odorous secretions 73
be changed to full species. Litoria raniformis,L. moorei and L. alboguttata,all
members of the L. aurea group, have similar acrid, menthol smells. The closely
related L. electrica and L. rubella also have indistinguishable odours. Conversely,
three species of medium-sized brown tree frogs, L. adelaidensis,L. ewingi and
L. rubella all smell grass-like, yet do not share a species group, while L. ewingi
and L. jervisiensis, two frogs morphologically similar and within the same species
group, smell very differently: the former emitting a “grassy” smell and the latter a
“curry” smell (Martin and Littlejohn, 1966).
Although further work is needed to determine whether such similarities and
differences in odour can be used to classify the relationships of frogs, it is
nonetheless interesting to consider odour relationships where the classification
is questionable. One area where we have applied odour characterisation is in
the Cyclorana platycephala/Litoria alboguttata debate. The observed odour for
C. platycephala lends weight to the personal view of M.J.T. that this species should
be classified as a monotypic genus. Maxson et al. (1982) questioned whether
C. platycephala formed an independent off-shoot of Cyclorana or whether it had
affinity with the L. aurea species group. Based on immunological data, the latter
seems more likely. Maxson et al. (1985) could not support the association of
C. australis and C. platycephala, demonstrating that C. platycephala is remote from
all congeners. This is also the case for its gross morphology, as C. platycephala has
a flattened head, prominent eyes, and fully webbed toes: these adaptations seem
aquatic rather than fossorial.
A similar case may be presented by Litoria alboguttata, a frog nearly identical in
form and habit to most Cyclorana. Originally described as Mitrolysis alboguttata by
Günther (1873) and considered a Cyclorana species by Parker (1940), this species
was moved to the genus Litoria on the basis of its intercalary structures (Tyler,
1974). Karyotypic studies by King et al. (1979), MC’F analyses by Maxson et al.
(1982) and morphological data by Burton (1996) and Meyer et al. (1997), however,
demonstrate a close relationship to C. australis and C. novaehollandiae, supporting
the return of the species to the genus Cyclorana. The production of an extremely
strong and overpowering odour, similar to that produced by L. aurea,L. moorei and
L. raniformis (L. aurea species group), by the species alboguttata argues against
such a move and supports Tyler’s classification.
No striking behavioural or ecological differences seem to exist between the
species of Cyclorana,andL. alboguttata. In all species the calls are long and of
low frequency; all species breed in ephemeral waters following heavy rains, and
breeding is opportunistic. Cyclorana have lentic tadpoles which are tolerant of high
water temperatures and which complete their development in six weeks or less.
Thus, biological differentiation does not appear to parallel described morphological
and biochemical differences. Many instances of the uncoupling of the evolution of
overall biology and molecular change have been reported. It has been suggested
that living in inhospitable areas with unreliable rainfall may account for similarities
noted in the overall biology of the various species of Cyclorana.

74 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
The greatest range of odours was observed in the hylid genus Litoria. Although
this perception may be an artefact of the greater number of species sampled
compared with other genera, the consistency of odours within other genera suggests
otherwise. This variation in odour fits with the current belief that the morphological,
biochemical, and biological attributes of Litoria are too extensive to maintain a
single genus. Despite the similarity in odour sensation this may also explain the
variation in odours produced by Limnodynastes. The discrete morphotypes within
that genus indicate the existence of at least three units and this is supported
by molecular data (Schäuble et al., 2000). The three units are the specialised
“bull frogs”, such as L. dorsalis sharing the dermal tibial gland, L. ornatus and
L. spenceri with polymorphic skin patterns and behavioural synapomorphies and a
conglomeration of non-fossorial taxa highly successful in radiating throughout vast
areas (Tyler, 1999).
Similar comparisons of non-Australian frog odours are difficult because only
small amounts of data on odorous species are available. In addition, there is a lack
of data on non-odorous animals. Of interest, however, is the detectable difference
between odours emitted by Rana luteiventris (new plastic) and the closely related
species R. pretiosa (bitter/spicy). Although discernable on the basis of allozymes,
species of the R. pretiosa complex are almost indistinguishable morphologically
(Green et al., 1997). Four measurements of the head — internarial distance,
interorbital distance, tympanum diameter, and orbital diameter — contribute the
greatest weight in distinguishing the species by multidiscriminate function analysis,
but the differences are small and not regarded as appropriate for qualitative
distinctions in the field (Green et al., 1997). The use of odour may be an effective
way to distinguish between both species.
The US Pacific Coast ranids R. a. aurora,R. muscosa and R. cascadae on the
other hand all appear to produce a ‘garlic’ aroma. All belong to the R. boylii species
group, which also includes R. pretiosa.R. pretiosa has been described as having a
bitter/spicy odour with a garlic-like note. Based on allozyme analysis R. cascadae
and R. aurora are closely allied, whilst R. pretiosa diverges considerably from the
other species. Morphologically, three of the species — R. aurora,R. cascadae
and R. pretiosa — may be considered generalised ‘brown frogs’, while R. boylii
and R. muscosa are morphologically divergent and may be termed ‘stream frogs’.
Furthermore, based on karyotypic character analysis, R. boylii and R. muscosa
appear to constitute a pair of sister taxa (Green, 1986a, b).
Mitochondrial DNA analysis, however, does not support a monophyly of R. boy-
lii and R. muscosa, favouring the hypothesis that R. aurora,R. cascadae and
R. muscosa form a clade. Analyses of nuclear ribosomal DNA restriction-site data
and allozymic data support a monophyletic R. boylii group, but do not effectively
resolve the relationships among the species within this group (Macey et al., 2001).
Care has to be taken in commenting on the relationships of Rana species. In certain
respects, karyotypic, morphotypic and genotypic evolution in these frogs may have
proceeded independently (Green, 1986a).

Frog odorous secretions 75
The odour of R. pretiosa was described as “similar to Bufo boreas but more
bitter and spicy”. This contrasts with the description of B. boreas producing a
“peanut paste” odour similar to B. punctatus.B. punctatus and B. boreas have
parapatric distributions in western North America and hybridisation is believed to
occur between both species. Both species, however, exhibit genetic divergence that
corresponds to their morphological divergence. This level of genetic differentiation
is greater than any reported for a hybridising pair of terrestrial vertebrates and as
such B. punctatus and B. boreas have been aligned with different clades (Feder,
1979).
Although odour comparisons provide support for a number of phylogenetic rela-
tionships, at present too little is known about the factors affecting the biochemistry
of granular glands to allow meaningful generalizations. For example, Myers et al.
(1978) noted a decline in the toxicity of secretions produced by Phyllobates terri-
billis maintained in captivity, which was later linked to the presence, or lack thereof,
of a dietary source (Daly et al., 1980). There even may be differences in the pres-
ence of a substance in secretions from glands on different parts of the body in the
same species. Serotonin was identified in the secretions of parotoid glands of Bufo
alvarius, but was absent from the macrogland on the hindlimb (Cannon et al., 1978).
Such analysis is further limited by the subjectivity of odour description, the fact that
odours detected by humans may constitute only a portion of the volatile compounds
released by frogs and, in the case of the Australo-Papuan anurans, the uncertainty
and incomplete knowledge of their phylogeny (pers. comm. M. Davies, Adelaide
University, September 2001).
It is clear that frogs produce a wide range of odours. The functions of these odours
may vary between taxa and in some cases odorous secretions may play multiple
roles in a frog’s life history. The association of odours with stressed and challenged
animals, however, suggests one function may be defence. While some of the odours
were considered pleasant (e.g. L. paraewingi and N. pictus), many were repulsive
or unbearable to be near (e.g. L. alboguttata,L. chloris,L. peroni and N. cen-
tralis). Whether such odours have similar effects on frog predators is conjectural.
It is easy to attribute an anti-predator function to odours that were repulsive by our
assessment. The production of volatile compounds that repel predators would confer
a selective advantage, even if frogs also produced non-volatile skin compounds
that were distasteful. By deterring predators at a distance frogs avoid mouthing or
handling by attackers assessing their palatability. Alternatively, odours may function
by acting as a cue to the predators that the prey is noxious. If predators learn that an
unpalatable prey is associated with a certain odour, they may avoid prey with that
odour in the future, even if the odour itself is benign (Williams et al., 2000). The
advantage of such chemical aposematism is that it could operate at night, as opposed
to aposematic colouration or postures, the effectiveness of which are dependent on
vision (Eisner et al., 1977; Eisner and Grant, 1981).
The use of aposematic odours also raises the possibility of mimicry. There are
advantages in smelling like a toxic and unpalatable species if it prevents attack from

76 Benjamin P.C. Smith, Craig R. Williams, Michael J. Tyler, Brian D. Williams
a predator. For instance, a number of Uperoleia and Geocrinia species superficially
resemble frogs of the toxic genus Pseudophryne and release indistinguishable,
earthy odours. This similarity in appearance and odour may be of advantage to the
frogs. Pseudophryne accumulate and produce lipophilic alkaloids (pumiliotoxins
and pseudophrynamines) in their skin secretion (Spande et al., 1988; Daly et al.,
1990; Smith et al., 2002). Despite similarities in their biology, such compounds are
absent in the secretions of both Uperoleia and Geocrinia (Daly et al., 1990; Smith
et al., 2002). Given the sympatry of many species in each of these three genera it is
hypothesised that they are involved in a mimetic relationship, but further tests are
needed to establish this.
Frogs may also use their odours as a form of camouflage. Presumably, the prey
of predators which hunt by smell can be cryptic and well protected if they have
the same smell as their immediate environment (Edmunds, 1974). Thus the ‘green’
grass-like and plant-like odours of many of the tree-frogs and the earthy odours
of the burrowing frogs Limnodynastes and Uperoleia could help ensure the frogs
remain undetected.
These same odours, whilst protecting the individual, may function as alarm
pheromones for nearby conspecifics, which may have evolved behavioural changes
(e.g. fleeing behaviour, change in shelter use) in response to these signals (Lutter-
schmidt et al., 1994; Marvin and Hutchison, 1995). A similar system has evolved in
the tadpoles of some species in response to water-borne chemical cues (e.g. Hews,
1988; Semlitsch and Gavasso, 1992). We have observations that suggest the odour
of the brown or Whistling tree-frog, Litoria ewingi, may function in such a capacity.
Often non-stressed frogs will emit distress calls in a manner identical to that emit-
ted when the species is touched by a cat (Tyler, 1976) when placed in contact with
recently secreted animals.
Odours released by frogs could also be involved in kin recognition, thereby
playing a role in social behaviours such as congregation or mate choice. Similar
systems making use of water-borne chemical cues exist in the tadpoles of some
species (Blaustein and O’Hara, 1982; Blaustein and Waldman, 1992; Blaustein and
Walls, 1995). Although we only detect odours when frogs are agitated it is possible
that smaller amounts of the same substances (in concentrations imperceptible to us)
are being released constantly and are integral to behaviour unrelated to predator
repulsion or avoidance. This supposition is supported by the observation that male
Rana muscosa produce strong garlic-like odours during the breeding season (Daerr,
2002). Such use of intraspecific pheromonal communication may be particularly
important amongst those species in which males lack vocal sacs and produce “soft”
calls detectable to the human ear at only a few metres. Visual communication
by arm and leg signalling often followed by tactile contact has been reported in
several species. Odoriferous compounds may serve as an initial attractant to bring
the animals into sufficient proximity for such activity. Injured and microbe/parasite
infested frogs have also been observed to release odours (pers. comm. D. Pergolotti,

Frog odorous secretions 77
Cairns Frog Hospital, September 2000), suggesting odour could be an important
cue to the health status of a potential mate.
Aside from the role volatile secretions may play in frog biology, odorants secreted
by frogs are an untapped source of bioactive compounds. Potential human uses
may become evident by studying the biological role of frog odorous secretions. For
instance it has been observed that the odorous secretion of L. caerulea is repellent
to mosquitoes (Cawood, 1997) and toxic to blowflies (Williams et al., 1998) and the
volatile secretion of L. ewingi has both antimicrobial action and is repellent against
a range of potential predators and parasites including snakes, rats and mosquitoes
(Smith, 2001). Furthermore, by describing the sensory effect of amphibian odours,
information about the physiological significance of the odour may be obtained
and thus lead to the isolation of pharmacologically active compounds (O’Mahony,
1986).
While this study provides a platform upon which further studies can be based,
it should be recognised that odours detected by humans may constitute only a
portion of the volatile compounds released by frogs. Accordingly, any contrast
between taxa based on human olfactory perception may be incomplete. Sensitive
chemical analysis techniques involving gas chromatography are required for the
total characterisation of frog odours. The interspecific variation revealed in this
study does, however, lend support to the use of odour in field identification.
Finally, although we recognise that people may disagree with some of our odour
classifications, in providing this review we hope to have drawn attention to what we
feel is an important topic and, in doing so, open up what has been a poorly explored
field of research.
Acknowledgements. We thank Hamilton Laboratories for financial support for
this study. Further support was provided to CRW by the Commonwealth National
Teaching Company Scheme. We also thank the Parks and Wildlife Commission of
the Northern Territory, The Western Australian Department of Conservation and
Land Management, The Queensland National Parks and Wildlife Service and the
South Australian Department of Environment and Natural Resources for permission
to collect and study the frogs used in this project. Our research was undertaken under
the provisions of the University of Adelaide’s Animal Ethics and Human Ethics
Approval committees. We are indebted to everyone who responded to our survey on
odorous frogs and to Mr. Steve Walker for his field assistance, Mr. K.R. McDonald
and Dr. M. Davies for specimens from Queensland and Prof. Ed Brodie Jr. for
helpful discussions on the topic of amphibian odours.
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Accepted: March 9, 2004.