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. References ANDUAGA, S. & HALFFTER, G., 1991. Escarabajos asociados a madrigueras de roedores (Coleoptera: Scarabaeidae, Scarabaeinae). Folia Entomol. Mex., 81: 185-197. ÁVILA,J. M., SANDOVAL, P., SCHMIDT, J. & SANCHEZ-PINERO, F., 1988. Contribución al conocimiento de los Scarabaeoidea (Coleoptera) coprófagos de los excrementos de conejo de la provincia de Granada. (España). Elytron, 2: 41-50. Bnz, A., 1988. Selección de macrohábitat por algunas especies y análisis de una comunidad de escarabeidos coprófagos (Coleoptera) del macizo de Ayllón (Sistema Central, España). Annales de la Société Entomologique de france (N.S.), 24: 203-210. BROOKS, D. R. & MACLENNAN., D. A., 1991. Phylogeny, Ecology and Behaviour. A research programme in Comparative Biology. University of Chicago Press, Chicago. CAMBEFORT, Y., 1991a. Dung beetles in tropical savannas. In: Dung Beetle Ecology: 156-178 (1. Hanski &Y. Cambefort, Eds.). Princeton University Press, New Jersey. - 1991b. From saprophagy t o coprophagy. In: Dung Beetle Ecology: 22-35 (l. Hanski & Y. Cambefort, Eds.). Princeton University Press, New Jersey. G. M. & FABBRI, M., 1983. ColeoCARPANETO, tteri Scarabaeidae e Aphodiidae coprofagi Miscel.lania Zoologica 19.1 (1996) associti agli escrementi dell'orso marsicano (Ursus arctos marsicanus Altobello) nel parco nazionale dlAbruzzo. Boll. Ass. Romana Entomol., 38: 31-45. CARPANETO, G. M . & PIATELLA,E., 1986. Studio ecologico su una comunita d i Coleotteri Scarabeoidei coprofagi nei Monti Cimini. Boll. Assoc. Romana Entomol., 40: 31-58. DESIERE,M . & THOMÉ,J. P., 1977. Variations qualitatives et quantitatives de quelques populations de coléopteres coprophiles associées aux excréments de trois types d'herbivores. Rev. Écol. Biol. Sol, 14(4): 583-591. DI CASTRI,F., 1990. On invading species and invaded ecosystems: the interplay of historical chance and biological necessity. In: Biological lnvasions in Europe a n d Mediterranean Bassin: 3-16 ( F. d i Castri, A. J. Hansen & M. Debussche, Eds.). Kluwer Academic Publishers, Dordrecht. DOUBE,B. M., 1983. The habitat prefer- ence o f some bovine dung beetles (Coleoptera: Scarabaeidae) in Hluhluwe Game Reserve, South Africa. Bulletin o f Entomological Research, 73: 357-371. FINCHER, G. T., 1981. The potential value of dung beetles in pasture ecosystems. J. Georgia Entomol. Soc., 16: 316-333. FINCHER, G. T., STEWART, T. B. & DAVIS,R., 1970. Attraction of coprophagous beetles t o faeces of various animals. J. Parasitol., 56: 378-383. GALANTE E., GARC~A-ROMAN M., BARRERA l. & GALINDO P., 1991. Comparison of spatial distribution patterns of dung-feeding scarabs (Coleoptera: Scarabaeidae, Geotrupidae) in a wooded and open pastureland i n the Mediterranean «Dehesa» area of the lberian Peninsula. Environmental Entomology, 20 (1): 90-97. E., MENA,J. & LUMBRERAS, C., 1995. GALANTE, Dung beetles (Coleoptera: Scarabaeidae, Geotrupidae) attracted t o fresh cattle dung in wooded and open pasture. Environmental Entomology, 24 (5): 1063-1068. GOLJAN, A., 1953. Studies on polish beetles o f the Onthophagus ovatus (L.) group w i t h some biological observations o n coprophagans (Col., Scarabaeidae). Annls. Mus. Zool. Polonici, 25: 55-81. GORDON, R. D., 1983. Studies on the genus Aphodius of the United States and Canada (Coleoptera: Scarabaeidae). VII. Food and habitat; distribution; key t o eastern species. Proc. Entomol. Soc. Wash., 85 (4): 633-652. GREENHAM, P. M., 1972. The effects of the variability of cattle dung on the multiplication o f t h e bushfly (Musca vetustissima Walk.). J. Anim. Ecol., 41: 153-166. HALFFTER, C., 1959. Etología y paleontología de Scarabaeinae. Ciencia (Méx.), 19: 165-178. - 1991. Historical and ecological factors determining the geographical distribution of beetles (Coleoptera: Scarabaeidae: Scarabaeinae). Folia Entomol. Mex., 82: 195-238. HALFFTER, G. M., FAVILA, E. & HALFFTER, V., 1992. A comparative study of the structure of the scarab guild in mexican tropical rain forests and derived ecosystems. Folia Entomol. Mex., 84: 131-156. HALFFTER, G. & MATTHEWS, E. G., 1966. The Natural History of Dung Beetles of the Subfamily Scarabaeinae (Coleoptera, Scarabaeidae). Folia Entomol. Mex., 1214: 1-312. HANCOX,M., 1991. The insect fauna of badger dung. Entomologist's Monthly Magazine, 127: 251. HANSKI,l., 1983. Distributional ecology and abundance of dung and carrionfeeding beetles (Scarabaeidae) in tropical rain forest in Sarawak, Borneo. Acta Zool. Fenn., 167: 1-45. - 1987. Nutritional ecology of dung- and carrion-feeding insects. In: Nutritional Ecology o f Insects, Mites, a n d Spiders: 837-884 (F. Slansky, Jr., & J. C. Rodríguez, Eds.). Wiley, New York. - 1989. Dung Beetles. In: Ecosystems o f the World, 14b, Tropical Forests: 489511(H. Lieth & J. A. Wagner, Eds.). Elsevier, Amsterdam. HANSKI,l. & CAMBEFORT, Y., 1991. Resource Martín-Piera & Lobo Partitioning. In: Dung Beetle Ecology: 330-365( 1. Hanski & Y. Cambefort, Eds.). Princeton University Press, New Jersey. HANSKI, l. & KUUSELA, S., 1983. Dung beetle communities in the Aland archipelago. Acta Entomol. Fenn., 42: 36-42. HOWDEN, H. F. & NEALIS,V. C., 1975. Effects of clearing in a tropical rain forest on the composition of the coprophagous scarab beetles fauna (Coleoptera). Biotropica, 7(2): 77-83. HURLBERT, S. H., 1978. The measurement of niche overlap and some relatives. ECOIO~Y, 59: 67-77. H., BALSBAUGH, E. U. & MACDANIEL, KESSLER, B., 1974. Faunistic comparison of adult coleoptera recovered from cattle and sheep manure in east-central South Dakota. Entomological News, 85: 67-71. T. J., 1986. KIRK, A. A. & RIDSDILL-SMITH, Dung beetles distribution patterns in the lberian Peninsula. Entomophaga, 31: 183-190. LANDIN,B. O., 1961. Ecological studies of dung beetles. Opusc. Entomol. (Suppl.), 19: 1-227. Loeo, J. M., 1985. Algunos datos y observaciones sobre la influencia del origen del excremento en la estructura de las comunidades de Scarabaeoidea (Coleoptera) coprófagos. Bolm. Soc. port. Ent., 3 (suppl. 1): 45-55. - 1992. Algunas consideraciones morfométricas sobre los Scarabaeoidea coprófagos (Col.). Zool. Baetica, 3: 59-68. - 1993. Estimation of dung beetles biomass (Coleoptera: Scarabaeoidea). Eur. J. Entomol., 90: 235-238. LOBO,J. M., MART~N-PIERA, F. & COCA-ABIA, M., 1992. Hábitos necrófagos en Scarabaeus cicatricosus (Lucas, 1846). Eos, 68: 202-203. Loeo, J. M., MART~N PIERA,F. & VEIGA,C. M., 1988. Las trampas pitfall con cebo, sus posibilidades en el estudio de las comunidades coprófagas de Scarabaeoidea (Col.); 1: Características determinantes de su capacidad de captura. Rev. Écob Biol. Sol, 25: 77-100. Loeo, J. M., SANMART~N, l. & MART~N-PIERA, F., (in press). Spatial turnover and diversity of dung beetle communities in a protected area of South Europe (Doñana National Park -Huelva, Spain). Ecologie. LOFTUS, R. T., MACHUGH,D. E., BRADLEY, D. E., SHARP P. M. & CUNNINGHAM, P., 1994. Evidence for t w o independent domestications of cattle. Proc. Natl. Acad. Sci, USA, 91: 2757-2761. LUMARET, J. P., GALANTE, E., LUMBRERAS, C., MENA,J., BERTRAND, M., BERNAL, J. L., COOPER, J. F., KADIRI,N. & CROWE,D., 1993. Field effects of ivermectin residues on dung beetles. J. Apll. Ecol., 30: 428-436. J. P. & IBORRA, O., (in press). SepaLUMARET, ration of trophic niches by dung beetles in overlaping habitats. Pedobiologia. LUMARET, J. P., KADIRI,N. & BERTRAND, M., 1992. Changes in resources: consequences for the dynamics of dung beetles communities. J. Appl. Ecol., 29: 349-356. J. P. & KIRK, A. A., 1987. EcolLUMARET, ogy of dung beetles in the French Mediterranean region (Coleoptera, Scarabaeidae). Acta Zoologica Mexicana (N.S.), 24: 1-55. - 1991. South temperate dung beetles. In: Dung Beetle Ecology: 97-1 15 (l. Hanski & Y. Cambefort, Eds.). Princeton University Press, New Jersey. LUDWIG,J. A. & REYNOLDS, J. F., 1988. Statistical Ecology. A primer o n methods a n d computing. John Wiley & Sons, New York. M A R T ~PIERA, N F., 1983. Composición sistemática y origen biogeográfico de la fauna ibérica de Onthophagini (Coleoptera, Scarabaeoidea). Boll. Mus. Reg. Sci. Nat. Torino, 1 (1): 165-200. MART~N PIERA,F. & ZUNINO,M., 1985. Taxonomie et biogéographie des Onthophagus du egroupe de 1'0. ovatusn (Coleoptera, Scarabaeoidea). Nouv. Revue Entomol., N.S., 2 (3): 241-250. MATTHIESSEN, J. N., 1982. The role of seasonal changes in cattle dung i n the population dynamics of the bush fly in South-western Australia. Proc. 3rd. Aust. Conf. Grassl. Invert. Ecol., Adelaide: 221-226. M ~ N K K ~ NM E .N&, WELSH,D. A., 1994. A 1 Miscel-lania Zoologica 19.1 (1996) biogeographical hypothesis o n t h e South-Western Australia. Bull. Soc. Entomol. Res., 76: 63-68. effects o f hurnan caused landscape SANCHEZ-PINERO, F. & ÁVILA, J. M., 1991. changes on the forest bird cornrnunities Análisis comparativo de los Scarabaeof Europe and North Arnerica. Ann. Zool. Fennici, 31: 61-70. oidea (Coleoptera) coprófagos de las deyecciones de conejo [Oryctolagus MYSTERUD, l. & WIGER, R., 1976. Beetle fauna associated w i t h scats of Brown cuniculus (L.)] y de otros mamíferos. Estudio preliminar. Eos, 67: 23-34. bear (Ursus arctos) frorn Trysil, South Norway 1974. Norw. J. Ent., 23: 1-5. SCHOLTZ, C. H. & CHOW,S. L., 1995. The evolution of habitat use and diet in NIBARUTA, C.,1982. Étude écologique cornthe Scarabaeoidea: a phylogenetic apparée des dipteres et des coléopteres colonisant les excrernents de bovides proach. In: Biology, Phylogeny, a n d Classification o f Coleoptera. Vol 1: 354autochtones et alloctones en rnilieu 374 (J. Pakaluk & S. A. Slipinski, Eds.). tropical africain (Burundi) et en rnilieu Papers Celebrating the 80th Birthday ternpere (Belgique). Ph. D. Tesis, Université de Liege. of Roy A. Crowson, Muzeurn i lnstytut NIBARUTA, G., DESIERE, M . & DEBAERE, R., Zoologii PAN, Warszawa. STEWART, T. B., 1967. Food preferences o f 1980. Étude cornparée de la cornposition chirnique des excrernents coprophagous beetles w i t h special rede quelques grands rnarnrniferes ference t o Phanaeus spp. J. Georgia herbivores africains. Acta Zoologica e t Entomol. Soc., 2: 69-77. Pathologica Antverpiensia, 75: 59-70. VEIGA,C. M., 1985. Consideraciones sobre OSBERG, D. C., DOUBE, B. N. & HANRAHAMS, hábitos necrófagos en algunas especies S. A., 1994. Habitat specificity i n de Scarabaeoidea Laparosticti paleárAfrican dung beetles: The effect of soil ticos (Insecta, Coleoptera). Bolm. Soc. type o n the survival o f dung beetle port. Ent., 2 (supl. 1): .123-134. inrnatures (Coleoptera: Scarabaeidae). VEIGA,C., LOBO,J. M . & MART~N-PIERA, F., Tropical Zoology, 7: 1-10. 1989. Las trampas pitfall con cebo, PALESTRINI, C. & ZUNINO,M., 1985. Osservasus posibilidades en el estudio de las zioni su1 regirne alirnentare dell'adulto comunidades coprófagas de Scarabaei n alcune specie del genere Thorectes oidea (Col.); 11: Análisis de efectividad. Muls. (Coleoptera: Scarabaeoidea: Rev. Écol. Biol. Sol, 26 (1): 91-109. Geotrupidae). Boll. Mus. Reg. Sci. Nat. WALTER, PH., 1983. La part de la necrohagie Torino, 3(1): 183-190. dans le regirne alirnentaire des scaraPAULIAN,R., 1943. Les Coléopteres. Forbéides coprophages afro-tropicaux. mes-Moeurs-R6le. Payot ed., Paris. Bull. Soc. Zool., Fr., 108 (3): 397-402. A., 1982. Cornposi- WHITTAKER, PECK,S. B. & FORSYTH, R. H., 1965. Dorninance and tion, structure, and cornpetitive behavdiversity i n land plant cornrnunities. iour in a guild of Ecuadorian rain forest Science, 147: 250-260. dung beetles (Coleoptera; Scarabae- ZUNINO,M., 1984. Sisternatica generica de¡ idae). Can. J. Zool., 60: 1624-1634. Geotrupinae (Coleoptera, ScarabaeRAINIO, M., 1966. Abundance and phenooidea: Geotrupidae), filogenesi della logy of sorne coprophagous beetles in Sottofarniglia e considerazioni biogeodifferent kinds of dung. Ann. Zool. grafiche. Boll. Mus. Reg. Sci. Nat. ToriFennici, 3: 88-98. no, 2(1): 9-162. RIDSDILL-SMITH, T. J., 1986. The effect o f ZUNINO, M. & PALESTRINI,C., 1986. seasonal change in cattle dung on egg El comportamiento telefágico de production by t w o species o f dung Trypocoprispyrenaeus (Charp.) adulto. beetles (Coleoptera: Scarabaeidae) in Graellsia, 42: 205-21 6.