A comparative discussion of trophic preferences in dung beetle

Miscel.lania Zooloqica 19.1 (1996)
13
A comparative discussion of
trophic preferences in
dung beetle communities
F. Martín-Piera & J. M. Lobo
Martín-Piera, F. & Lobo, J. M., 1996. A comparative discussion of trophic preferences in
dung beetle communities. Misc. Zool., 19.1: 13-3 1 .
A cornparative discussion on trophic pre ferences in dung beetle cornrnunities.- Ava i la ble
information on trophic preferences of dung beetles (Scarabaeoidea) in different biogeographic
regions is reviewed. Trophic resource partitioning in a dung beetle (Coleoptera, Scarabaeoidea)
community in the ((Parque Nacional de Doñana)), Spain, was also studied, using nine
different kinds of wild and domestic vertebrate excrement as trap bait. Undifferentiated
attraction t o human and herbivore faeces was noted. Human and domestic ungulate
faeces was colonized by a richer fauna than that of wild herbivores, which was not the
specialized trophic adaptation of any species. Although polyphagy is the most common
feeding behaviour, the excrement of carnivores and other omnivores was hardly colonized. This pattern differs from that of other biogeographic regions. Negligible importance
of the trophic dimension on the structure of these communities may be due to the early
presence of man in the Palaearctic Region. Nevertheless, human interference alone cannot
have led to an absence of true polyphagy (undifferentiated attraction to al1 kinds of
faeces). Further research is suggested, aimed at determining whether observed resource
partitioning in dung beetles communities is a consequence of human colonization or is a
pre-Neolithic evolutionary event.
Key words: Dung beetles, Coleoptera, Scarabaeoidea, Trophic preferences, Resource partitioning, Ecological-historical causes.
(Rebut: 22 1 96; Acceptació condicional.. 29 V 96; Acc. definitiva: 18 VI 96)
Ferrnín Martln-Piera & Iorge M. Lobo, Depto. Biodiversidad y Biologla Evolutiva, Museo
Nacional de Ciencias Naturales -C.S./.C., dIosé Gutiérrez Abascal 2, 28006 Madrid, España
(Spain).
This work has been financed by Fauna Ibérica Project, D.G.I.C.Y.T. grant PB89-0081
@
1996 Museu de Zoologia
Martin-Piera & Lobo
(one o f t h e rnost irnportant wildlife
reserves i n the Mediterranean area),
The physical and chernical composition w i t h i n the locality of El Rocío, Huelva,
of herbivore faeces varies widely w i t h
UTM 29SQB2812 (Spain).
The sarnpling was taken i n a clearing
1987), and even w i t h
the species (HANSKI,
by rneans o f 15 pitfall traps set o u t ranseason within the sarne species, as a funcdomly on 60 x 40 m grid, average dist i o n of pasture quality (GREENHAM,
1972;
MATTHIESSEN,
1982; RIDSDILL-SMITH, 1986). Still tance between traps of 10 m, l e f t for
48 h (23-25 April, 1992).
greater variation occurs arnong the faeThe pitfall-traps were baited w i t h
ces of herbivores, ornnivores and carniapproxirnately 1,000 g of fresh excrernent
vores. In rnany cases it has been shown
that dung beetles are attracted differ- (see LOBOet al., 1988; VEIGAet al., 1989),
ently t o different types of faeces (PAUL~AN,except in the case of lynx and fox faecesbaited traps (250 g were used), d u e t o the
1943). It has been argued that trophic
scarcity of resources.
choice could play a role in deterrnining
Nine kinds of excrernent were used,
the coexistence of species of a dung
beetle cornrnunity, and their resource frorn vertebrates that still live in the reserve, ranging frorn herbivore (cow, horse,
partitioning.
deer and fallow deer); predorninantly herFew studies have been rnade o n the
bivore (wild boar); predorninantly carnitrophic preferences o f the Palaearctic
Region temperate biornes species, and vore (lynx, fox); t o ornnivore (rnan, badthese deal with the differential attraction ger).
Two traps were baited with each type
of the food resources of no more than
of faeces, except for those using faeces
four marnrnal species (LANDIN,1961; RAINIO,
frorn lynx, fox and rnan (table 1).
1966; DESIERE
& THOMÉ,1977; LOBO,1985;
CARPANETO
& PIATELLA,
1986; SANCHEZ-PINERO There is evidence in favour of a density of t w o traps per site being adequate
& ÁVILA,1991). With the exception of the
works by NIBARUTA
et al. (1980) and NIBARUTAt o have a good representation of the dung
beetle cornmunity structure in the Medi(1982), no joint study, using the faeces of
b o t h wild and dornestic rnarnrnals, has terranean regions. Such a density ensures
that about 53% of local spring species are
been rnade in this region.
captured (confidence intervals at 95% are
This paper atternpts t o determine
51.08-55.27%), these species representing
whether differences correlated w i t h faeces type exist in an lberian dung beetle 86% of total abundance and 85% of total biornass (Lobo & Lurnaret, in preparacornrnunity. Results are cornpared w i t h
those previously obtained in the sarne and tion).
A t the sarne time, sarnples were taken
other biogeographic regions to: i) verify
the irnportance of food preference results frorn one fresh cow-dung baited (1,000 g)
i n resource partitioning and ii) provide pitfall trap, set for 48 h in each of the
material for a discussion, frorn a histori- following eight park habitats: inter-sandcal point of view, of the extent t o which dune troughs devoid of vegetation ('corrales'); stationary dunes reforested w i t h
trophic preference may have conditioned
the present cornposition of these cornmu- pines; rnarsh; original holrn oak and cork
oak wood; rnarsh-holrn oak ecotone; scrub
nities.
fringes of semi-permanent lagoons ('lucio~');strearn bank prirnary and reforested
woods (table 2).
Material and Methods
The sarnples were examined t o deterThe study was carried o u t in or near a mine local fauna diversity, and t o obtain
grove o f holrn oaks on the northern an estirnate of the abundance and habit a t distribution of each species.
edge of 'Parque Nacional de Doñana'
lntroduction
Miscel.lania Zoologica 19.1 (1996)
15
Results
Whittaker's plots of species abundance
data (WHITTAKER,
1965) indicate: uneven
The number of individuals of each species distribution of abundance in the horse
collected with each type of bait i s shown dropping community (fig. 3), giving low
in table 1. As figure 1 shows, faeces bait eveness and diversity values; a more even
type fell into three groups, according t o distribution of abundance and greater
the number of species and individuals diversity, in cow, fallow deer and human
captured: group A, greatest richness and dung beetle communities; fewer species,
abundance (cow, human and one of the
none dominant, in deer and wild boar, and
horse dung); group B, medium to high thus high eveness and diversity values,
richness, lower abundance (three species along with an even species abundance
of wild herbivore and another horse drop- figures.
ping trap); group C, very poor both in
Faunal similarity found in the differdiversity and abundance (carnivores and ent types of faeces was cluster analysed,
badger). Total biomass (computations based using percent dissimilarity (PD) and
on length-body weight regressions; LOBO, UPGMA, flexible, weighted and unweigh1992, 1993) per group was also the great- ted centroid grouping strategies (LUDWIG
est for group A (fig. 2).
81 REYNOLDS, 1988). Dung beetle species
Number of Species
25
B
20 -
/
i
,A¿ííGG=.
\
fallow deer t
t wild boar
t deer
t horse
t deer
,*
15 í
;
k i l d boar
*
.'
L/--
lo-,'
5-
cow
i
t
COW t
__
\
human \,
---
--
*
\
t ,i
horse
------_/-/'
/,'
N
',
C
\%S--,
\ t iynx,
om e r
O
A
-----
i--_
i
-
-
A
I
I
I
I
100
200
300
400
500
Abundance
Fig. 1. Relationship between number of species and abundance for the 15
dung-baited pitfall traps belonging t o nine different dung types.
Relacíón entre e l número de especies y la abundancia para 15 trampas pítfall
cebadas con nueve tipos diferentes de excrementos.
Martín-Piera & Lobo
16
F1
F2 L Fo Hu Tot Nb
O
1
O
0
0
1
0
O
1 0 0 9 1 4 0 . 0 9
0
0
O
O
O
0
0
0
0
O
O
0
0
0
10.07
1
0
2
O
O
0
0
0
0
O
O
0
0
0
30.18
3
0
1
1
O
1
O 0 0 0 1 1
O
1
1
3
1
9
O
0
1
5
9 1 0 0
O
0
1
O
O
O
0
0
0
0
O
O
O
0
0
1
O
O
0
0
0
0
O
O
O
0
0
O
O
O
0
0
0
0
O
1
2
2
1
8
1
0
0
0
0
2
2
3 0 0 3 2 4 0 . 4 9
10 21 34
48
6
8
O
O 12
4
6
5 O
o
o
0
0
0
1
0
o
299 55134 188
5
3
O
O
6 74
38
77 O
023711160.42
23
29 O
O 63 3830.42
Scarabaeus cicatricosus
1
1
1
Copris hispanicus
O
Euoniticellus fulvus
Onthophagus furcatus
2
1
0
97 11 58
Caccobius schreberi
Aphodius baraudi
Faeces
Q W1 WZ 81 82 D1 02
0
H1 H2 C1
O 0 0
O
1180.26
O
1410.39
0
0
10.07
0
0
4
50.03
0
0
0
10.07
0
O 52 206 0.37
0
0
1
50.22
82
3
7
O
O 10
O
2
9 1 5
3
8
0
0
6 3 1 7 1 9 0 0 6 8 8 0 . 4 4
O
0
2
O
O
O
0
0
0
O
0
1
15
3
1 2 0
O
2
O
O
6
2
11
4
0
2
5
3
4
0
0
4
2
O
O
0
1 3 0
0
0
3018
018
910.50
0 0 0 1 1 3 5 0 . 3 7
1
0
6
5
O
0
0
0
1
0
4
5 0 0 0 2 2 0 . 2 7
O
0
1
O
O
1
0
0
0
1
1
O
0
0
0
40.50
1
0
0
O
O
1
0
0
0
0
O
O
0
0
1
30.25
O 0 1 2
3
O
O
0
0
0
0
2
0 0 0 0 1 7 0 . 1 1
2
1
1
3
3
O
2
0
0
0
0
3
7
O35
8
O
O
O
O
1
3
16
0
0
1160.44
4 0
O
4
780.30
1
0
0
o
o
1
0
0
0
0
O
O
0
0
0
20.21
O
0
1
o
o
0
0
0
0
0
1
O
0
0
0
20.21
6
127
20
1
3
O
O
O
0
0
O
O
O
0
0
4
2
12
1
0
O
O
0
0
1 3 0
0151040.38
0
0
10.07
0
0
10.07
fhorectes hispanicus
O
0
0
O
O
O
0
0
0
1
O
O
Typhaeus momus
2
2
2
4
O
1
O
0
0
0
O
2 1
461 103 365 445
27
64
O
O 61 104 174 201 1
1 470 2477
10
16
O
O 16 13
19
17 1
1 21
0.5 0.6
O
O 0.8 0.9
1.3
2.2 0.1 0.1 8.4 28.3
Total abundance
Total no. species
Total biomass
19 14 21
20
4.6 1.6 2 9 4.3
113280.21
35
Miscel.lania Zooloqica 19.1 (1996)
17
Table 1. Dung beetlss species caught w i t h pitfall traps baited w i t h faeces o f : H.
Wonie; C. Cow; W. Wild boar; B. Badger; D. Deer; F. Fallow deer; L. Lynx; Fo. Fox;
Hu. Humatn; Wb. WUR~BERT'S standardized niche breath (1978).
lnventarío de eole6pteros coprdfagos capturados con trampas p i t f a l l ceba&$ con heces de: W. Caballo; C. Vaca; W. Jabalí; B. Tejón; D. Ciervo; E Gamo; L.
Lince; E Zorro; Wu. Heces humanas; Nb. Amplitud de Nicho estandarizada de
HURLBPRT
(1978).
found in cow, human, horse, and t o a lesser
degree, fallow deer dung, were very similar (fig. 4). Associated w i t h them, fauna
found in wild boar and deer were also
similar. Only one species (Typhaeusmomus)
was n o t caught i n any other bait type
except in carnivore dung (lynx and fox).
This clustering pattern was always independent o f the grouping strategies used.
The null hypothesis of an equal probability of colonizing any faeces was estimated
using a X* test. Species abundance figures used
were restricted t o samples in which a$ least
one beetle was caught (n = 13), thus excluding badger-faeces fauna figures. Excepting
the case of Aphodius immundus Creutzer
(x2= 19.64, 0.5 > P > 0.1), al1 observed faeces abundance values differ significantly
Dung types
-j
A
human
cow
1
wy
yg
T/y
l**2;
....., ,
U
,?+a
~z
%p
~%,/7
~f/
A;Z&SB
horse
B
j w i l d boar
w i l d boar
T l y n x
GROUP
f0x
C
badger
i d g e r
O
2
4
6
Biomass (grs. d r y w e i g h t )
F1$. 2, ?@fa1b i o m & ~ captured
$
for t h e 15 dung-baited pitf
to ninl differerrt dung types.
Bf@m&$osst o b l conseguida para las 15 trampas p i t f a l l con nue
tcs ds excrementos.
8
1O
18
Martín-Piera & Lobo
Tabla 2. Species inventory o f dung beetles caught w i t h pitfall traps baited w i t h
cow dung, in the Parque Nacional de DoAana, Huelva (Spain): 1. Sandy dunes; 2.
Píne-reforested dunes; 3. Scrub; 4. Marsh-holm oak ecotone; 5. Marsh; 6. Holm
oak and cork oak clearing; 7. Pine-reforested clearing; 8. Stream bank woods.
Nb. HURLBERT'S
standardized niche breadth (1978).
Inventario de coleópteros coprófagos capturados con trampas p i t f a l l cebadas
con excrementos de vaca en e l Parque Nacional de Doiiana: 1 . Dunas; 2. Dunas
reforestadas con pinos; 3. Matorral; 4. Ecotono marisma-encinar; 5.Marisma; 6.
Claro en bosque mixto de encinas y alcornoques; 7. Claro en pinar de repoblación; 8. Bosque de ribera; Nb. Amplitud de nicho estandarizada de HURLBERT
(1978).
Abandance
- bumon
H'
E
1,98-2.07
0,53-0,62
1,84
0.47
Abandance
H'
1,28-2.42
wiidboar2,11-2.45
üorn 1,22-1,55
E
0,37 -0.92
1,17-0,95
0,48-0,54
1O0
1O0
10
1
Species Rank
Species Rank
Fig. 3. WHITTAKER'S
plots o f species abundance data (1965) for the six dung
types most colonized: H'. Shannon's index o f diversity; E. Evenness (Modified
Hill's ratio, LUDWIG& REYNOLDS, 1988). Except for human faeces, the species
abundance curve for every pair o f dung baited traps, are plotted.
Curvas de especies-abundancia ( W H ~ ~ A K1965)
E R , de los seis tipos de excrementos mds colonizados: H. índice de diversidad de Shannon; E. Equitatividad
& REYNOLDS,
1988). Se han ilustrado las curvas de
(Ratio de H i l l modificada, LUDW~G
abundancia para cada par de trampas, excepto en las heces humanas.
Miscel.lania Zooloqica 19.1 (1996)
13
122
243
49
O
O
7
O
434
0.20
12
6
11
3
1
O
O
O
33
0.39
Onrhophepus furcatus
1
O
4
O
O
1
1
O
O. maki
1
15
156
41
O
34
12
3
T m c&odognsnensis
O
1
O
O
O
O
O
O
T6ciE abeindance
52
217
830
608
45
365
189
23
2329
"i8W rgu&br of spedes
30
t3
15
24
10
21
20
7
34
Scwsrbaaus eicaiJicosus
S.
.,
19
wcer
-
70.27
262
0.26
10.06
Martín-Piera & Lobo
20
HUMAN
COW
HORSE
FALLOW
DEER
DEER
WlLD
BOARD
LYNX
FOX
BADGER
Fig. 4. Dendrogram o f t h e clustering o f níne dung types using the Percentage
Dissimilarity (PD) as measure of resembiance and UPGMA as clustering strategY.
Dendrograma de similitud faunística entre los nueve tipos de excrementos.
La medida de sJmilitud es e l Porcentaje de OisimJlaridad (PD) y la estrategia de
agrupamiento es UPGMA.
from values derived from equal probability hypothesis (P c 0.001 in al1 cases). Species trophic preference values can be determined from the ratio o f individuals
captured w i t h a given faeces t o total captures (fig. 5). Only in the cases of cow,
human, horse and fallow deer faeces were
species captured which accounted for more
than 25% of the total.
Thirty-one species were attracted t o
group A faeces, 30 t o group B, and only
one t o group C. Of the eight species captured i n only one faeces group, seven
consisted of three or fewer individuals,
and may be considered incidental captures.
Only the moderately abundant (n = 11)
A. merdarius (Fabricius) was captured exclusively in group A. The number of indiv i d u a l ~captured in group A and B was
used t o compare the average number of
individuals per dung type for species in
both groups. Data from the 18 species
w i t h an abundance 2 13 were used. This
figure is the minimum abundance of any
species evenly distributed in every dung- ;
baited trap, one beetle per trap. Species
found in both groups w i t h a significantly
different average number of individuals
per excrement were: Onthophagus maki
(Illiger) (t = 3.61, 0.002 c P e 0.01), 0. similis
(Scriba) ( t = 5.83, P e 0.001), 0. opacicollis
Reitter ( t = 7.48, P e 0.001), A. striatulus
Waltl (t = 2.35, P = 0.05),A. tersus Erichson
( t = 2.86, P = 0.02) and Typhaeus momus
(Olivier) (t = 2.31, P = 0.05). The figures
for A. scybalarius (Fabricius) (t = 2.19) and
A. baraudivillareal (t = 2.15) were at the
limit of statistical significance ( t = 2.262,
P = 0.05). The average number of indiv i d u a l ~of al1 these species was greatest
in group A, which means that around 40%
o f the sampled species were attracted
Miscel.lania Zoolosica 19.1 (1996)
21
Number of species
Fig. 5. Nurnber of species r e p r e s e n t d by more than 75%, between 50%-75%
and between 25%-50% o f total individuals in sorne of the six most colonized
dung types.
Número de especies representadas p o r más d e l 75%, entre e l 50 y a l 75% y
entre e l 25 y e l 50% d e l t o t a l d e individuos en algunos de los seis tipos de excrementos más colonirados.
w i t h greater frequency t o cow, hurnan and
horse faeces.
The richness and abundance of species
in the sarnpling frorn different habitats
(table 2) was very similar t o that of the
different bait types (table 1). Of the 38
species captured, only seven (18%) did not
belong t o both sarnplings. All these seven
species may be considered as incidental
captures (three or fewer individuals). There
is a highly significant correlation between
the nurnber of individuals of each species
,captured i n the t w o samplings (r = 0.613,
d f = 29, P < 0.001). HURLBERT'S
standardized niche breadth (1978) was calculated
using again the trophic and habitat data
of the 18 species w i t h an abundance 2
13, as rnentioned above (tables 1 and 2),
giving uncorrelated values (r = -0.03, d f
= 16, NS). The rnean trophic niche breadth
(I S.E.) value (0.35 I0.03) was found t o
be rather higher than that of the rnean
habitat niche breadth (0.24 I0.02).
High species abundance vahes correlate
with wide trophic niche breadths, while low
values are uncorrelated (fig. 6A). Sixteen of
the 18 species (n 2 13) were found in at least
five faeces (sirnplifying the data by excluding
the contribution from lynx, fox and badger).
Only A. erraticus (L.) (n = 22) and A. ictericus
(Laicharting) (n = 17) seerned t o dernonstratea
rnarked trophic predilection for cow dung.
Martín-Piera & Lobo
22
Abundance
0,l
0.2
0,3
0,4
Trophic niche breadth
Biomass (mgrs. dry weight)
10003
O
0,l
0,2
0.3
0,4
0,5
Trophic niche breadth
Fig. 6. Rela.tionship between trophic niche breadth al: species and its: A.
Abundance; B. Dry weight. (Niche breadth measured with HWRLBERT'S
standardized niche breadth, 1978).
Relación entre la amplitud de nicho trófico de las especies y su: A. Abundancia; B. Peso seco. (Amplitud de nicho calculada mediante el índice de HURLBERT,
1978).
Miscel.lania Zoologica 19.1 (1996)
Asian and South Arnerican tropical forest species are specialized in feeding on
Table 3. Total abundance and total
carrion
or faeces, but about one half of
biornass for five trophic niche breath
these
species
rnake equal use of carrion
ranges (HURLBERT,
1978).
1991);
and dung (HANSKI,1983; HALFFTER,
Abundancia t o t a l y biomasa t o t a l
whereas in Africa, where carrion i s not
existente para cinco rangos de
amplitud de nicho trófico (HURLEERT, cornrnonly a dung beetle resource, species are norrnally restricted t o the con1978).
surnption of herbivore and ornnivore dung
(CAMBEFQRT,
1991a; HANSKI
& CAMBEFORT,
1991).
In the African continent, the presence
of rnany large carnivores, coupled w i t h
carrion birds (vultures), leave little carrion available for beetles. The situation
is the reverse in South America. Furthermore, competition between beetles and
flies for carrion i s higher i n Africa than
in Arnerica (Lumaret, pers. cornrn.). The
fact that the cornposition and volatile
substances of decornposing carrion are
more like those of ornnivore than herbivore dung (HANSKI,1987), coupled w i t h
the relative nurnerical scarcity of herbivore and omnivore rnarnrnals in Asian and
There was no correlation between spe- Arnerican tropical forests, has given rise,
cies dry weight and trophic niche breadth according t o sorne authors (HALFFTER
&
i n which 18 species (fig. 6B), b u t it i s in- MATTHEWS,
1966; HANSKI& CAMBEFORT,
1991;
HALFFTER,
teresting t o note that Scarabaeus cica1991), t o necrophagous trophisrn.
tricosus (ball roller) and 1 momus (ballSirnilarly, dung beetle species i n North
carrier; see ZUNINO
& PALESTRINI,
1986), the Arnerica are attracted t o al1 kinds o f caronly large sized species, were among those
nivore, herbivore and ornnivore dung. The
three w i t h the narrowest trophic niche cornrnunities inhabiting different types
breadth. While niche breadth gradually
of faeces can be dissirnilar and frequently
increased with total abundance, total cap- dung beetle species are spatially restricted
tured biornass did not (table 3).
by faeces availability (GORDON,
1983). Sorne
cornrnunities rnake use of only such herbivore dung as that of rodents (ANDUAGA
Discuasion
& HALFFTER,
1991). More than 40% of Western United States species are linked w i t h
A general review on trophic preferences
rodents or turtles (GORDON,
1983). Ornnio f dung beetles
vore dung has been found t o be most
coprophagan-attracting in North Arnerica,
Species o f Scarabaeidae i n the tropics while that of herbivores and carnivores
frequently show copro-necrophagous
attracts a similar nurnber of dung beetles
feeding habits (HANSKI,1989; WALTER,
(STEWART,
1967; FINCHERet al., 1970).
1983),
and specialized trophic preferences preFeeding patterns of the dung beetle
dorninantly occur (HALFFTER,
1959; HALFFTERcornmunities inhabiting Palaearctic tem& MATTHEWS,
1966). Carnivore dung fauna
perate biomes seern t o be quite differi n such regions are rnade up of dung ent. The Doñana experirnent suggests t w o
beetles attracted t o carrion and herbivprincipal dung groups depending on their
ore dung (HANSKI,1987). In Southeast faunal composition: herbivore and hu-
Martín-Piera & Lobo
man faeces on the one hand; and the car- of dung, such as rabbit (MARTIN-PIERA,
1983;
nivore and wild omnivores on the other
ÁVILAet al., 1988; SANCHEZ-PINERO
& ÁVILA,
hand, characterized by a poor attractive1991; LUMARET
& IBORRA,
in press).
ness. Palaearctic dung beetle fauna are
lnteresting accounts of faunal changes
not commonly found in carnivore or wild
in pastureland, related with livestock
omnivore faeces, and those so found al- changes, have been published. Replaceways also occur i n herbivore dung (MYSTE- ment of sheep w i t h cattle brings w i t h it
RUD & WIGER,
1976; CARPANETO
& FABBRI,1983;
a more hydrated, abundant and less epheHANCOX,
1991; HALFFTER
& MATTHEWS,
1966). mera1 resource. Subsequent qualitative
European dung beetles only sporadically,
variation in dung beetle community comand never exclusively, consume carrion
position has not been observed, but in(VEIGA,1985; LOBO
et al., 1992) but only as creased total dung beetle biomass and
adult food. In this case, carrion would
abundance has been, along w i t h alterarepresent a nitrogen-rich resource of which tions in the relative frequency of species
the mobile adults may take advantage
(LUMARET
et al., 1992). According t o other
(HANSKI
& CAMBEFORT,
1991). However, i f the comparisons of faunal composition in the
cattle dung chemical cornposition changes, t w o types of dung (KESSLER
et al., 1974;
w i t h more amino-acids, dung beetles are
HANSKI
& KUUSELA,
1983), communities have
more numerously attracted and dung i s been found t o be similar, though poorer
attractive for a longer period (LUMARET
et and w i t h uneven species abundance real., 1993).
lationship in sheep dung. Ecologically, the
Doñana data indicate that: i) cow and drier and more ephemeral resource prohuman dung are consumed by most of vides for fewer opportunities or niche dispecies represented by their largest abunmensions, thus limiting the number o f
dances and biomass; ii) horse and fallow
coexisting species. Therefore, the data
deer communities are similar t o cow and suggest that species coexistence is much
human dung communities, b u t the spe- more dependent o n the availability of an
cies abundance relationship in horse drop- adequate dung-type variety than dungpings i s uneven due the dominant con- choice. When different kinds of excrements
tribution of 0. sirnilis, 0. opacicollis and coexist in the same area, it is reasonable
O. rnaki populations; iii) fallow deer com- t o suppose that opportunities for most
munities present very even species abun- species increase.
dance relationship; iv) much lesser use i s
Other studies have indicated that prefmade of dung of other herbivores.
erence for precisely one type of herbivHuman dung, exerting the greatest co- ore dung may depend on species size and
prophagous attraction in the tropics (PECK trophic-reproductive behaviour, or may be
& FORSYTH, 1982; HOWDEN
& NEALIS,1975;
influenced by: the relation between the
HALFFTER
et al., 1992), seems t o be as copro- dung water content and the climate; maphagous-attracting as herbivore dung in nageability and consistency; or the seatemperate biomes (RAINIO,1966; FINCHERet
sonal availability of dung (GOLJAN,
1953;
al., 1970), and thus, i s t h e only omnivore
LAND~N,
1961; RAINIO, 1966; LOBO,1985).
dung t o play such a role there.
The individuals of species (except one)
Significant variation o f dung beetle captured for the present study were not
community w i t h herbivore food type i n randomly distributed among the six prinnorthern and temperate Europe is not dis- cipal dung bait types, thus demonstrating
cernible in published data (LANDIN,1961; trophic preference. More than 50% of A.
RAINIO, 1966; LOBO,1985; CARPANETO
& PIATELLA, ictericus, A. lineolatus l lliger and A. erraticus
1986; KIRK & RIDSDILL-SMITH,
1986; LUMARETwere found in cow dung; S. cicatricosus
& KIRK,1991). Only some singular species
(Lucas), T: rnornus and A. rnerdarius in huare sapro-coprophagous (PALESTRINI
& ZUNINO, man dung; Euoniticellus fulvus (Goeze) in
1985), or are linked t o a particular type fallow deer droppings (belonging t o the 18
Miscel.lania Zoologica 19.1 (1996)
species each accounting for more than 5%
of total individuals, table 1). More than
25% o f the individual total o f these 18
species were found in cow, human, horse
and fallow deer dung alone, along with
the greatest number of wide trophic niche
breadth species. Sixteen of these 18 species were found in at least five of the six
most attracting dungs (cow, horse,'fallow
deer, wild boar, deer and human). As previously mentioned abundance and trophic
niche breadth are related in such a way that
large population species are also broad
trophic spectrum.
In the temperate latitudes of Palaearctic
Region, species are not trophically segregated, generally making use o f both
herbivore and human dung, while still
preferring some particular type. Our data
indicate that the most coprophage attracting faeces are those with greatest richness, abundance and biomass, exerting
equal attraction on small population species. For this reason, populations were
larger in group A faeces for those species captured in significantly unequal nurnbers in groups A and B. No more than three
individuals, of species exclusive t o group
B were captured. Put another way, less rich
herbivore dung fauna is an impoverished
fauna of the more potent coprophagan
attracting faeces; which means that there
is no fauna exclusive t o wild herbivore
faces, colonized by domestic mammal and
human dung fauna.
25
tat distribution in Doñana varies from
et al.,
Scarabaeidae t o Aphodiidae (LOBO
in press) and can be a function of variables other than food source; for example soil texture, tolerance t o
waterlogging and waterholding soil
capacities (OSBERG
et al., 1994), and vegetative cover (DOUBE,
1983; LUMARET
& KIRK,
et al., 1991,
1987; BAZ, 1988; GALANTE
1995). Iiowever, choice o f a particular
type of dung could be conditioned by
the habitat preference o f i t s vertebrate
source.
Species body size or average weight i s
unrelated t o degree of attraction t o faeces types. As seen earlier, polyphagy in
species making use of herbivore faeces i s
normal, so it i s not surprising that numbers o f both species and individuals increase considerably with increased trophic
niche breadth (table 3). Nevertheless,
biomass seems t o be more evenly distributed among the different trophic categories (generalists and specialists), due t o
the contribution o f the few large body
size, stenophagan species. Of the three
narrow trophic niche, abundant population species, t w o are large body size, the
ball-roller S. cicatricosus and the ball-carrier T. momus. These species are captured
most often in human dung, perhaps attracted by i t s high nitrogen content. Ac& CAMBEFORT
(1991), ballcording t o HANSKI
rollers compensate food quantity restrictions imposed by transportion over distances from source by generally choosing
nutrient-rich omnivore dung.
Habitat, body size and trophic preferences
The fauna attracted t o different kinds
o f faeces is highly representative of the
Doñana National Park, estimated species
populations being similar. Generally
speaking, species segregation i s more a
function of differences o f habitat than
in trophic resource (greater mean niche
breadth), so the lack o f correlation between trophic and habitat niche breadth
should not surprise. The ability t o survive in a variety of environments is unrelated t o trophic niche breadth. Habi-
Trophic generalists and effect of human
colonization
Dung beetle community resource partitioning in the Palaearctic Region i s not
shown by available data t o be greatly
affected by trophic selection. Preferences
that do exist can vary in time and space,
depending on dung environment interactions. Unlike the cases o f tropical regions and North America, carnivore and
non-human omnivore dung attract dung
Martín-Piera & Lobo
beetles only slightly, or not at all, and est destruction in the eastern regions of
& WELSH,
1994).
wild herbivore dung fauna seems t o be North America (MONKKONEN
If Palaearctic Region community struca sub-group of cornmunities that make
use o f hurnan and domestic rnammal ture before the Neolithic period was similar t o that of other regions today, why
dung. Everything suggests, therefore, an
are there no carnivore dung beetles? Is
undifferentiated attraction towards the
effluents and the volatile components this an empty niche? Have specialist speof the different types o f herbivore fae- cies, or true generalists, feeding on herbivore, carnivore and wild omnivore dung,
ces. Why are the temperate biomes of
the Palaearctic Region different? Why i s become extinct? Human intervention
could have reduced the habitat of these
polyphagy common in herbivore dung
species? Why are coprophagan not at- vertebrates, but where it still exists, there
tracted t o carrion or carnivore and om- should be associated dung beetle fauna.
Recent historical changes in community
nivore dung?
Man's presence in the Palaearctic Re- structure, due t o human impact, would
gion over so many years may have made not completely account for the lack of
dung beetle community structure less sen- these specialist and truly generalist spesitive t o the trophic dimension. The most cies. These changes should have occurred
i n pre-Neolithic times. In other words,
widely held view i s that domestication of
livestock goes back t o 10,000-8,000 years could these singular dung beetle fauna
BP (LOFTUS
et al., 1994). Furthermore, ma- date from pre-human colonization of the
Palaearctic ternperate regions?
jor changes in European forests (frorn forest
It has recently been argued that taxot o predominantly open cultivated lands),
nomic differences between European and
started as early as 10,000-8,000 years ago
North American avifauna stem frorn both
in the Mediterranean area and about 5,000
years ago in Western and Central Europe the geographical configuration (particularly topographical) of the continental land
(MONKKONEN
& WELSH,
1994 and references
therein). Old World mammal populations masses and events during the Pleistocene
(MONKKONEN
& WELSH,1994). Unlike the
would thus have been modified throughPalaearctic Region, orientation of the
out the Neolithic period by human activNearctic mountain ranges has favoured
ity, especially livestock herding, possibly
leading t o drastic reduction, or even ex- temperate and tropical biota exchange.
These authors point out that birds of the
tinction, of specialized dung beetles, as well
Nearctic Region show a wider life history
as major dietary restrictions in the truly
range, a higher number of specialized spetrophic generalist species (carnivore, wild
ornnivore and herbivore feeding dung) as cies, and a greater between-habitat component of biodiversity. Whereas habitat
a response t o resource scarcity. Potentially,
generalism and colonizing abilities were
more herbivore-polyphagous species would
selected from among western Palaearctic
have prospered, and possibly extended their
species, which have experienced fragmengeographic range. If, as in other continents,
trophic specialist andlor truly generalist Pa- tation and loss of forest habitats, first nalaearctic dung beetle fauna existed, then turally and later human-induced many
today's cornmunities would have been struc- times during the past t w o million years
& WELSH,
1994). Could the sarne
tured over time, by human activity, so much (MONKKONEN
causes explain the ecological trophic patso that in American and Australian regions,
less affected until recently by human ac- tern of coprophagous Scarabaeoidea, in
both Palaearctic and Nearctic regions?
tivity, it has been necessary t o irnport dung
On the other hand, Mediterranean ecobeetles t o degrade domestic livestock faeces. In USA, grazing mammals were first systems have been invaded and colonized
introduced about 200-300 years ago (FINCHER, several times in geological and historical
terms by generalist invader species of dif1981), coinciding with the large-scale for-
Miscel.lania Zoologica 19.1 (1996)
ferent biogeographical origin (DI CASTRI,
1990). lberian Onthophagini illustrates a
good exarnple of coexisting lineages corning frorn different biogeographical origins (MARTIN
PIERA,1983). In this historical context, it can also been hypothetized
that old invader dung beetle comrnunities structured by true generalists feeding o n al1 kind of available faeces and
strict specialists, would have been substituted for new invaders better adapted
t o the opening o f t h e new adaptative
zone provided by Artiodactyls dung
(CAMBEFORT,
1991b; SCHOLTZ & CHOW,19951,
and t o the Pleistocene habitat fragrnentation (MONKONEN
& WELSCH,
1994).
To test the idea that the lack of specialist and true generalist dung beetle
fauna is either the result o f pre-Neolithic
evolutionary events or Neolithic ecologic
changes in the Palaearctic Region, three
cornplernentary approachesare suggested;
t w o ecological and one phylogenetic.
1. If hurnan activity has favoured today's
frequent and abundant species, through
sustained, intense rnodification of available trophic source type and frequency,
dung beetle comrnunity structure changes
should be observed in areas nearly free of
hurnan influence. However, it will not be
easy t o find a site for testing this hypothesis, because of the lack of truly non-hurnan-transformed ecosysterns in the Western Palaearctic Region.
2. If the rich local Palaearctic dung beetle
cornrnunity's null (or nearly null) attraction toward carnivore and wild ornnivore
dung i s the result o f singular evolutionary adaptations, rather than a response
t o resource scarcity, then this trophic behaviour was probably a pre-Neolithic adaptation originated before those vertebrate populations decreased.
3. Establishing trophic adaptation age:
Polarizing the polyphagy-stenophagy i n
the prirnitive derived sense could be inferred frorn a reconstruction o f t h e
phylogenetic relationships arnong species,
and rnapping on t o the cladograrn one
or t h e other trophic pattern (BROOKS
&
MCLENNAN,
1991). A phylogenetic approach
27
t o the habitat use and diet of rnajor Scarabaeoidea's lineages using this rnethodology, has been recently proposed by SCHOLTZ
& CHOWN
(1995).
Available phylogenetic inferences of
Palaearctic coprophagous Scarabaeidae
indicate repeated establishment of trophic
specializations in several lines: prirnarily in
ancestral groups such as the rnost prirnitive
Geotrupinae (genera Lethrus, Typhaeus,
Thorectes; see ZUNINO,1984); secondarily in
sorne ancient Palaearctic radiations of the
genus Onthophagus (Scarabaeidae). with
few representativestoday, such as Parentius,
and Palaeonthophagus of the latigena
group (MART~N
PIERA
& ZUNINO,1985).
Thus i f t h e rnost specialized trophic
adaptations are confined t o high-rank taxa
(genera, subgenera and species groups),
Palaearctic Region trophic structuring can
be inferred t o date, at the latest, frorn
before appearance of the hurnan.
Conclusions
1. In the ternperate Palaearctic Region,
trophic choice little influences Scarabaeoidea
dung beetle cornmunity resource partitioning. Species are generally attracted t o
hurnan and al1 types of herbivore faeces.
Thus, polyphagy restricted t o these kinds
of excrernents is the generalized condition.
Species segregation i s generaily more
influenced by habitat than trophic
resource.
2. Both large- and srnall-population
species are rnost attracted t o hurnan and
dornestic rnarnrnal faeces. There is n o exclusively wild herbivore faeces fauna, but
rather an irnpoverished one, in cornparison
w i t h that o f hurnan and dornestic ungulate faeces. Carnivore faeces are hardly
colonized at all.
3. The lengthy duration o f the effects
o f the hurnan presence in the Palaearctic
Region rnay explain why coprophagous
Scarabaeoidea cornrnunity structure is nearly
independent of trophic choice. However,
the human irnpact alone, historically recent, does not explain the observed ab-
Martín-Piera & Lobo
sence of a true polyphagy in the regional
coprophagous Scarabaeoidea, extremely
poor in communities that colonize carnivore and wild omnivore faeces.
Resumen
Discusión comparada sobre las preferencias tróficas en comunidades de escarabajos coprófagos
Se estudia la relevancia de la dimensión
trófica en el reparto de recursos, en una
comunidad ibérica de escarabeidos
coprófagos en el Parque Nacional de
Doñana. Se analizaron nueve clases diferentes de excrementos de vertebrados
domésticos y salvajes (tabla 1). Los resultados indicaron que existe una atracción
indiferenciada a todo tipo de heces de
herbívoros y deyecciones humanas (fig.
1, tabla 2). Sin embargo, aunque la
eurifagia en este tipo de heces es la condición generalizada, los excrementos de
carnívoros y otros omnívoros, apenas son
colonizados (fig. 2). No existe una fauna
exclusiva de las deyecciones de herbívoros salvajes. Se trata de una fauna empobrecida respecto a la que coloniza las heces
humanas y las de ungulados domésticos
(figs. 3-6).
Este patrón difiere del que se conoce
en otras regiones biogeográficas. Se argumenta que la antigüedad de la transformación antrópica en la Región Paleártica,
puede explicar la escasa importancia de la
dimensión trófica en la estructura de estas comunidades. Sin embargo, la intervención humana no acaba de explicar la ausencia de una verdadera polifagia, es decir, la colonización indiscriminada de todo
tipo de excrementos.
Se sugieren algunas líneas de investigación alternativas que permitirían evaluar
s i la actual estructuración de las comunidades coprófagas, respecto al factor recurso, es un evento histórico reciente de origen antrópico o, por el contrario, se trata
de un evento preneolítico, cuyas causas
habrían de investigarse a escala evolutiva.
Acknowledgements
The authors wish t o thank M n Milagro
Coca (Museo Nacional de Ciencias
Naturales; C.S.I.C.) and Alberto Donaire
(Estación Biológica de Doñana, C.S.I.C.),
for their help w i t h the field work, and
Domingo Iglesias Fuente, Research
granted student in the Museo Nacional
de Ciencias Naturales, 1992, for his assistance in laboratory and office. To Mr.
James Cerne for his revision of different
English drafts.
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