A Comparative Discussion of Trophic Preferences in Dung Beetle Communities

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 to 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 lntroduction (one of the rnost irnportant wildlife reserves in the Mediterranean area), The physical and chernical composition within the locality of El Rocío, Huelva, of herbivore faeces varies widely with UTM 29SQB2812 (Spain). the species (HANSKI,1987), and even with The sarnpling was taken in a clearing season within the sarne species, as a func- by rneans of 15 pitfall traps set out ran- tion of pasture quality (GREENHAM,1972; domly on 60 x 40 m grid, average dis- MATTHIESSEN,1982; RIDSDILL-SMITH, 1986). Still tance between traps of 10 m, left for greater variation occurs arnong the fae- 48 h (23-25 April, 1992). ces of herbivores, ornnivores and carni- The pitfall-traps were baited with vores. In rnany cases it has been shown approxirnately 1,000 g of fresh excrernent that dung beetles are attracted differ- (see LOBOet al., 1988; VEIGAet al., 1989), ently to different types of faeces (PAUL~AN,except in the case of lynx and fox faeces- 1943). It has been argued that trophic baited traps (250 g were used), dueto the choice could play a role in deterrnining scarcity of resources. the coexistence of species of a dung Nine kinds of excrernent were used, beetle cornrnunity, and their resource frorn vertebrates that still live in the re- partitioning. serve, ranging frorn herbivore (cow, horse, Few studies have been rnade on the deer and fallow deer); predorninantly her- trophic preferences of the Palaearctic bivore (wild boar); predorninantly carni- Region temperate biornes species, and vore (lynx, fox); to ornnivore (rnan, bad- these deal with the differential attraction ger). of the food resources of no more than Two traps were baited with each type four marnrnal species (LANDIN,1961; RAINIO, of faeces, except for those using faeces 1966; DESIERE& THOMÉ,1977; LOBO,1985; frorn lynx, fox and rnan (table 1). CARPANETO& PIATELLA, 1986; SANCHEZ-PINERO There is evidence in favour of a den- & ÁVILA,1991). With the exception of the sity of two traps per site being adequate works by NIBARUTAet al. (1980) and NIBARUTAto have a good representation of the dung (1982), no joint study, using the faeces of beetle cornmunity structure in the Medi- both wild and dornestic rnarnrnals, has terranean regions. Such a density ensures been rnade in this region. that about 53% of local spring species are This paper atternpts to determine captured (confidence intervals at 95% are whether differences correlated with fae- 51.08-55.27%), these species representing ces type exist in an lberian dung beetle 86% of total abundance and 85% of to- cornrnunity. Results are cornpared with tal biornass (Lobo & Lurnaret, in prepara- those previously obtained in the sarne and tion). other biogeographic regions to: i) verify At the sarne time, sarnples were taken the irnportance of food preference results frorn one fresh cow-dung baited (1,000 g) in 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-sand- cal point of view, of the extent to which dune troughs devoid of vegetation ('co- trophic preference may have conditioned rrales'); stationary dunes reforested with the present cornposition of these cornmu- pines; rnarsh; original holrn oak and cork nities. oak wood; rnarsh-holrn oak ecotone; scrub fringes of semi-permanent lagoons ('lu- cio~');strearn bank prirnary and reforested Material and Methods woods (table 2). The sarnples were examined to deter- The study was carried out in or near a mine local fauna diversity, and to obtain grove of holrn oaks on the northern an estirnate of the abundance and habi- edge of 'Parque Nacional de Doñana' tat distribution of each species. 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 is 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 to 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 differ- diversity 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 unweigh- 1992, 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 2 5 - - A ----- \ human \, B cow t \ 20 - / COW t * ,A¿ííGG=. i \ i--___ horseti , fallow deer t i ------_/-/' t wild boar i 15 - t deer t horse í ; t deer ,* kild boar A /,' lo-,' * N,' L/--.'

5- C \%S--, \ t iynx,

o mer I I I I O 100 200 300 400 500 Abundance

Fig. 1. Relationship between number of species and abundance for the 15 dung-baited pitfall traps belonging to nine different dung types. Relacíón entre el número de especies y la abundancia para 15 trampas pítfall cebadas con nueve tipos diferentes de excrementos. 16 Martín-Piera & Lobo

Faeces H1 H2 C1 Q W1 WZ 81 82 D1 02 F1 F2 L Fo Hu Tot Nb Scarabaeus cicatricosus 110 O 1 O0010 O 1009140.09 100 O O O0000 O O000 10.07 Copris hispanicus O10 2 O O0000 O O000 30.18 Euoniticellus fulvus 30 11O 1 O00011 O00 1180.26 O 11 3 19O0 15 9100 O 1410.39 O01 O O O0000 O O000 10.07 O00 1 O O0000 O O004 50.03 O00 O O O0000 O 1000 10.07 Onthophagus furcatus 22 181 00002 2 3003240.49 10 21 34 48 6 8 O O 12 4 6 5 O O 52 206 0.37 210 o o 00010 o O001 50.22 299 55134 188 5 3 O O 6 74 38 77 O 023711160.42 97 11 58 82 3 7 O O 10 O 23 29 O O 63 3830.42 O 2 915 3 800 631719006880.44 O02 O O O0000 1 O000 3018 Caccobius schreberi 15 3 120 O 2 O O 6 2 11 130 018 910.50 Aphodius baraudi 402 5 3 40042 O 00011350.37 106 5 O 00010 4 5000220.27 O01 O O 10001 1 O000 40.50 100 O O 10000 O O001 30.25 O012 3 O O0000 2 0000170.11 113 3 O 20000 3 200 1160.44 7 O35 8 O O O O 1316 40 O 4 780.30 100 o o 10000 O O000 20.21

O01 o o 00000 1 O000 20.21 6 127 20 1 3 O O 4 2 12 130 0151040.38 O00 O O O0010 O O000 10.07 fhorectes hispanicus O00 O O O0001 O O000 10.07 Typhaeus momus 2 2 2 4 O 1 O000 O 21 113280.21 Total abundance 461 103 365 445 27 64 O O 61 104 174 201 1 1 470 2477 Total no. species 19 14 21 20 10 16 O O 16 13 19 17 1 1 21 35 Total biomass 4.6 1.6 2 9 4.3 0.5 0.6 O O 0.8 0.9 1.3 2.2 0.1 0.1 8.4 28.3 Miscel.lania Zooloqica 19.1 (1996) 17

Table 1. Dung beetlss species caught with pitfall traps baited with faeces of : 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 pitfall 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 to a lesser The null hypothesis of an equal probabil- degree, fallow deer dung, were very simi- ity of colonizing any faeces was estimated lar (fig. 4). Associated with them, fauna using a X* test. Species abundance figures used found in wild boar and deer were also were restricted to samples in which a$ least similar. Only one species (Typhaeusmomus) one beetle was caught (n = 13), thus exclud- was not caught in any other bait type ing badger-faeces fauna figures. Excepting except in carnivore dung (lynx and fox). the case of Aphodius immundus Creutzer This clustering pattern was always inde- (x2= 19.64, 0.5 > P > 0.1), al1 observed fae- pendent of the grouping strategies used. ces abundance values differ significantly

Dung-- types j human 1

wyygT/y?azp ,/7fl**2; A cow ....., ,U,+~%~%~/A;Z&SB

horse B

j wild boar wild boar Tlynx GROUP f0x C badger idger

O 2 4 6 8 1 O Biomass (grs. dry weight)

F1$. 2, ?@fa1biom&~$ captured for the 15 dung-baited pitf to ninl differerrt dung types. Bf@m&$osstobl conseguida para las 15 trampas pitfall con nue tcs ds excrementos. 18 Martín-Piera & Lobo

Tabla 2. Species inventory of dung beetles caught with pitfall traps baited with 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'Sstandardized niche breadth (1978). Inventario de coleópteros coprófagos capturados con trampas pitfall cebadas con excrementos de vaca en el 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 repobla- ción; 8. Bosque de ribera; Nb. Amplitud de nicho estandarizada de HURLBERT(1978).

H' E H' E Abandance Abandance

1,98-2.07 0,53-0,62 1,28-2.42 0,37 -0.92 wiidboar2,11-2.45 1,17-0,95 - bumon 1,84 0.47 üorn 1,22-1,55 0,48-0,54 1 O0 1O0

1 Species Rank Species Rank

Fig. 3. WHITTAKER'Splots of species abundance data (1965) for the six dung types most colonized: H'. Shannon's index of diversity; E. Evenness (Modified Hill's ratio, LUDWIG& REYNOLDS, 1988). Except for human faeces, the species abundance curve for every pair of dung baited traps, are plotted. Curvas de especies-abundancia (WH~~AKER,1965) de los seis tipos de excrementos mds colonizados: H. índice de diversidad de Shannon; E. Equitatividad (Ratio de Hill modificada, LUDW~G& REYNOLDS, 1988). Se han ilustrado las curvas de abundancia para cada par de trampas, excepto en las heces humanas. Miscel.lania Zooloqica 19.1 (1996) 19

Scwsrbaaus eicaiJicosus 13 122 243 49 O O 7 O 434 0.20 S. wcer 12 6 11 3 1 O O O 33 0.39

Onrhophepus furcatus 1 O 4 O O 11O 70.27 O. maki 1 15 156 41 O 34 12 3 262 0.26

Tmc&odognsnensis O 1 O O O O O O 10.06 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 ., 20 Martín-Piera & Lobo

HUMAN COW HORSE FALLOW DEER WlLD LYNX FOX BADGER DEER BOARD

Fig. 4. Dendrogram of the clustering of níne dung types using the Percentage Dissimilarity (PD) as measure of resembiance and UPGMA as clustering strat- egY. Dendrograma de similitud faunística entre los nueve tipos de excrementos. La medida de sJmilitud es el Porcentaje de OisimJlaridad (PD) y la estrategia de agrupamiento es UPGMA.

from values derived from equal probabil- both groups. Data from the 18 species ity hypothesis (P c 0.001 in al1 cases). Spe- with an abundance 2 13 were used. This cies trophic preference values can be de- figure is the minimum abundance of any termined from the ratio of individuals species evenly distributed in every dung- ; captured with a given faeces to total cap- baited trap, one beetle per trap. Species tures (fig. 5). Only in the cases of cow, found in both groups with a significantly human, horse and fallow deer faeces were different average number of individuals species captured which accounted for more per excrement were: Onthophagus maki than 25% of the total. (Illiger) (t = 3.61, 0.002 c P e 0.01), 0. similis Thirty-one species were attracted to (Scriba) (t = 5.83, P e 0.001), 0. opacicollis group A faeces, 30 to group B, and only Reitter (t = 7.48, P e 0.001), A. striatulus one to group C. Of the eight species cap- Waltl (t = 2.35, P = 0.05),A. tersus Erichson tured in only one faeces group, seven (t = 2.86, P = 0.02) and Typhaeus momus consisted of three or fewer individuals, (Olivier) (t = 2.31, P = 0.05). The figures and may be considered incidental captures. for A. scybalarius (Fabricius) (t = 2.19) and Only the moderately abundant (n = 11) A. baraudivillareal (t = 2.15) were at the A. merdarius (Fabricius) was captured ex- limit of statistical significance (t = 2.262, clusively in group A. The number of indi- P = 0.05). The average number of individual~captured in group A and B was vidual~of al1 these species was greatest used to compare the average number of in group A, which means that around 40% individuals per dung type for species in of the sampled species were attracted Miscel.lania Zoolosica 19.1 (1996) 21

Number of species

Fig. 5. Nurnber of species representd by more than 75%, between 50%-75% and between 25%-50% of total individuals in sorne of the six most colonized dung types. Número de especies representadas por más del 75%, entre el 50 y al 75% y entre el 25 y el 50% del total de individuos en algunos de los seis tipos de excrementos más colonirados.

with greater frequency to cow, hurnan and of the 18 species with an abundance 2 horse faeces. 13, as rnentioned above (tables 1 and 2), The richness and abundance of species giving uncorrelated values (r = -0.03, df in the sarnpling frorn different habitats = 16, NS). The rnean trophic niche breadth (table 2) was very similar to that of the (I S.E.) value (0.35 I 0.03) was found to different bait types (table 1). Of the 38 be rather higher than that of the rnean species captured, only seven (18%) did not habitat niche breadth (0.24 I0.02). belong to both sarnplings. All these seven High species abundance vahes correlate species may be considered as incidental with wide trophic niche breadths, while low captures (three or fewer individuals). There values are uncorrelated (fig. 6A). Sixteen of is a highly significant correlation between the 18 species (n 2 13) were found in at least the nurnber of individuals of each species five faeces (sirnplifying the data by excluding ,captured in the two samplings (r = 0.613, the contribution from lynx, fox and badger). df = 29, P < 0.001). HURLBERT'Sstandard- Only A. erraticus (L.) (n = 22) and A. ictericus ized niche breadth (1978) was calculated (Laicharting) (n = 17) seerned to dernonstrate a using again the trophic and habitat data rnarked trophic predilection for cow dung. 22 Martín-Piera & Lobo

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'Sstand- ardized niche breadth, 1978). Relación entre la amplitud de nicho trófico de las especies y su: A. Abun- dancia; B. Peso seco. (Amplitud de nicho calculada mediante el índice de HURLBERT, 1978). Miscel.lania Zoologica 19.1 (1996)

Asian and South Arnerican tropical for- Table 3. Total abundance and total est species are specialized in feeding on biornass for five trophic niche breath carrion or faeces, but about one half of ranges (HURLBERT,1978). these species rnake equal use of carrion Abundancia totaly biomasa total and dung (HANSKI,1983; HALFFTER,1991); existente para cinco rangos de whereas in Africa, where carrion is not amplitud de nicho trófico (HURLEERT, cornrnonly a dung beetle resource, spe- 1978). cies are norrnally restricted to the con- surnption of herbivore and ornnivore dung (CAMBEFQRT,1991 a; HANSKI& CAMBEFORT,1991 ). In the African continent, the presence of rnany large carnivores, coupled with carrion birds (vultures), leave little carrion available for beetles. The situation is the reverse in South America. Further- more, competition between beetles and flies for carrion is higher in 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 with 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 to sorne authors (HALFFTER& in which 18 species (fig. 6B), but it is in- MATTHEWS,1966; HANSKI& CAMBEFORT,1991; teresting to note that Scarabaeus cica- HALFFTER,1991), to necrophagous trophisrn. tricosus (ball roller) and 1 momus (ball- Sirnilarly, dung beetle species in North carrier; see ZUNINO& PALESTRINI,1986), the Arnerica are attracted to al1 kinds of car- only large sized species, were among those nivore, herbivore and ornnivore dung. The three with 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 West- ern United States species are linked with A general review on trophic preferences rodents or turtles (GORDON,1983). Ornni- of dung beetles vore dung has been found to be most coprophagan-attracting in North Arnerica, Species of Scarabaeidae in the tropics while that of herbivores and carnivores frequently show copro-necrophagous attracts a similar nurnber of dung beetles feeding habits (HANSKI,1989; WALTER,1983), (STEWART,1967; FINCHERet al., 1970). and specialized trophic preferences pre- Feeding patterns of the dung beetle dorninantly occur (HALFFTER,1959; HALFFTERcornmunities inhabiting Palaearctic tem- & MATTHEWS,1966). Carnivore dung fauna perate biomes seern to be quite differ- in such regions are rnade up of dung ent. The Doñana experirnent suggests two beetles attracted to carrion and herbiv- principal 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 attractive- 1991; 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. Replace- ways also occur in herbivore dung (MYSTE- ment of sheep with cattle brings with it RUD & WIGER,1976; CARPANETO& FABBRI, 1983; a more hydrated, abundant and less ephe- HANCOX,1991; HALFFTER& MATTHEWS, 1966). mera1 resource. Subsequent qualitative European dung beetles only sporadically, variation in dung beetle community com- and never exclusively, consume carrion position has not been observed, but in- (VEIGA,1985; LOBOet al., 1992) but only as creased total dung beetle biomass and adult food. In this case, carrion would abundance has been, along with altera- represent a nitrogen-rich resource of which tions in the relative frequency of species the mobile adults may take advantage (LUMARETet al., 1992). According to other (HANSKI& CAMBEFORT,1991). However, if the comparisons of faunal composition in the cattle dung chemical cornposition changes, two types of dung (KESSLERet al., 1974; with more amino-acids, dung beetles are HANSKI& KUUSELA,1983), communities have more numerously attracted and dung is been found to be similar, though poorer attractive for a longer period (LUMARETet and with uneven species abundance re- al., 1993). lationship in sheep dung. Ecologically, the Doñana data indicate that: i) cow and drier and more ephemeral resource pro- human dung are consumed by most of vides for fewer opportunities or niche di- species represented by their largest abun- mensions, thus limiting the number of dances and biomass; ii) horse and fallow coexisting species. Therefore, the data deer communities are similar to cow and suggest that species coexistence is much human dung communities, but the spe- more dependent on the availability of an cies abundance relationship in horse drop- adequate dung-type variety than dung- pings is 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- to suppose that opportunities for most munities present very even species abun- species increase. dance relationship; iv) much lesser use is Other studies have indicated that pref- made of dung of other herbivores. erence for precisely one type of herbiv- Human 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 HALFFTERet al., 1992), seems to be as copro- dung water content and the climate; ma- phagous-attracting as herbivore dung in nageability and consistency; or the sea- temperate biomes (RAINIO,1966; FINCHERet sonal availability of dung (GOLJAN,1953; al., 1970), and thus, is the only omnivore LAND~N,1961; RAINIO, 1966; LOBO,1985). dung to play such a role there. The individuals of species (except one) Significant variation of dung beetle captured for the present study were not community with herbivore food type in randomly distributed among the six prin- northern 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 hu- are sapro-coprophagous (PALESTRINI& ZUNINO, man dung; Euoniticellus fulvus (Goeze) in 1985), or are linked to a particular type fallow deer droppings (belonging to the 18 Miscel.lania Zoologica 19.1 (1996) 25

species each accounting for more than 5% tat distribution in Doñana varies from of total individuals, table 1). More than Scarabaeidae to Aphodiidae (LOBOet al., 25% of the individual total of these 18 in press) and can be a function of vari- species were found in cow, human, horse ables other than food source; for ex- and fallow deer dung alone, along with ample soil texture, tolerance to the greatest number of wide trophic niche waterlogging and waterholding soil breadth species. Sixteen of these 18 spe- capacities (OSBERGet al., 1994), and veg- cies were found in at least five of the six etative cover (DOUBE,1983; LUMARET& KIRK, most attracting dungs (cow, horse,'fallow 1987; BAZ, 1988; GALANTEet al., 1991, deer, wild boar, deer and human). As pre- 1995). Iiowever, choice of a particular viously mentioned abundance and trophic type of dung could be conditioned by niche breadth are related in such a way that the habitat preference of its vertebrate large population species are also broad source. trophic spectrum. Species body size or average weight is In the temperate latitudes of Palaearctic unrelated to degree of attraction to fae- Region, species are not trophically seg- ces types. As seen earlier, polyphagy in regated, generally making use of both species making use of herbivore faeces is herbivore and human dung, while still normal, so it is not surprising that num- preferring some particular type. Our data bers of both species and individuals in- indicate that the most coprophage attract- crease considerably with increased trophic ing faeces are those with greatest rich- niche breadth (table 3). Nevertheless, ness, abundance and biomass, exerting biomass seems to be more evenly distrib- equal attraction on small population spe- uted among the different trophic catego- cies. For this reason, populations were ries (generalists and specialists), due to larger in group A faeces for those spe- the contribution of the few large body cies captured in significantly unequal nurn- size, stenophagan species. Of the three bers in groups A and B. No more than three narrow trophic niche, abundant popula- individuals, of species exclusive to group tion species, two are large body size, the B were captured. Put another way, less rich ball-roller S. cicatricosus and the ball-car- herbivore dung fauna is an impoverished rier T. momus. These species are captured fauna of the more potent coprophagan most often in human dung, perhaps at- attracting faeces; which means that there tracted by its high nitrogen content. Ac- is no fauna exclusive to wild herbivore cording to HANSKI& CAMBEFORT(1991), ball- faces, colonized by domestic mammal and rollers compensate food quantity restric- human dung fauna. tions imposed by transportion over dis- tances from source by generally choosing nutrient-rich omnivore dung. Habitat, body size and trophic preferences

The fauna attracted to different kinds Trophic generalists and effect of human of faeces is highly representative of the colonization Doñana National Park, estimated species populations being similar. Generally Dung beetle community resource parti- speaking, species segregation is more a tioning in the Palaearctic Region is not function of differences of habitat than shown by available data to be greatly in trophic resource (greater mean niche affected by trophic selection. Preferences breadth), so the lack of correlation be- that do exist can vary in time and space, tween trophic and habitat niche breadth depending on dung environment inter- should not surprise. The ability to sur- actions. Unlike the cases of tropical re- vive in a variety of environments is un- gions and North America, carnivore and related to trophic niche breadth. Habi- non-human omnivore dung attract dung Martín-Piera & Lobo beetles only slightly, or not at all, and est destruction in the eastern regions of wild herbivore dung fauna seems to be North America (MONKKONEN& WELSH, 1994). a sub-group of cornmunities that make If Palaearctic Region community struc- use of hurnan and domestic rnammal ture before the Neolithic period was simi- dung. Everything suggests, therefore, an lar to that of other regions today, why undifferentiated attraction towards the are there no carnivore dung beetles? Is effluents and the volatile components this an empty niche? Have specialist spe- of the different types of herbivore fae- cies, or true generalists, feeding on her- ces. Why are the temperate biomes of bivore, carnivore and wild omnivore dung, the Palaearctic Region different? Why is become extinct? Human intervention polyphagy common in herbivore dung could have reduced the habitat of these species? Why are coprophagan not at- vertebrates, but where it still exists, there tracted to carrion or carnivore and om- should be associated dung beetle fauna. nivore dung? Recent historical changes in community Man's presence in the Palaearctic Re- structure, due to 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 spe- sitive to the trophic dimension. The most cies. These changes should have occurred widely held view is that domestication of in pre-Neolithic times. In other words, livestock goes back to 10,000-8,000 years could these singular dung beetle fauna BP (LOFTUSet al., 1994). Furthermore, ma- date from pre-human colonization of the jor changes in European forests (frorn forest Palaearctic ternperate regions? to predominantly open cultivated lands), It has recently been argued that taxo- started as early as 10,000-8,000 years ago nomic differences between European and in the Mediterranean area and about 5,000 North American avifauna stem frorn both years ago in Western and Central Europe the geographical configuration (particu- (MONKKONEN& WELSH, 1994 and references larly topographical) of the continental land therein). Old World mammal populations masses and events during the Pleistocene would thus have been modified through- (MONKKONEN& WELSH, 1994). Unlike the out the Neolithic period by human activ- Palaearctic Region, orientation of the ity, especially livestock herding, possibly Nearctic mountain ranges has favoured leading to drastic reduction, or even ex- temperate and tropical biota exchange. tinction, of specialized dung beetles, as well These authors point out that birds of the as major dietary restrictions in the truly Nearctic Region show a wider life history trophic generalist species (carnivore, wild range, a higher number of specialized spe- ornnivore and herbivore feeding dung) as cies, and a greater between-habitat com- a response to resource scarcity. Potentially, ponent of biodiversity. Whereas habitat more herbivore-polyphagous species would generalism and colonizing abilities were have prospered, and possibly extended their selected from among western Palaearctic geographic range. If, as in other continents, species, which have experienced fragmen- trophic specialist andlor truly generalist Pa- tation and loss of forest habitats, first na- laearctic dung beetle fauna existed, then turally and later human-induced many today's cornmunities would have been struc- times during the past two million years tured over time, by human activity, so much (MONKKONEN& WELSH, 1994). Could the sarne so that in American and Australian regions, causes explain the ecological trophic pat- less affected until recently by human ac- tern of coprophagous Scarabaeoidea, in tivity, it has been necessary to irnport dung both Palaearctic and Nearctic regions? beetles to degrade domestic livestock fae- On the other hand, Mediterranean eco- ces. 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 1981), coinciding with the large-scale for- terms by generalist invader species of dif- Miscel.lania Zoologica 19.1 (1996) 27 ferent biogeographical origin (DI CASTRI, to the habitat use and diet of rnajor Scara- 1990). lberian Onthophagini illustrates a baeoidea's lineages using this rnethodol- good exarnple of coexisting lineages corn- ogy, has been recently proposed by SCHOLTZ ing frorn different biogeographical ori- & CHOWN(1995). gins (MARTINPIERA, 1983). In this histori- Available phylogenetic inferences of cal context, it can also been hypothetized Palaearctic coprophagous Scarabaeidae that old invader dung beetle comrnuni- indicate repeated establishment of trophic ties structured by true generalists feed- specializations in several lines: prirnarily in ing on al1 kind of available faeces and ancestral groups such as the rnost prirnitive strict specialists, would have been sub- Geotrupinae (genera Lethrus, Typhaeus, stituted for new invaders better adapted Thorectes; see ZUNINO,1984); secondarily in to the opening of the new adaptative sorne ancient Palaearctic radiations of the zone provided by Artiodactyls dung genus Onthophagus (Scarabaeidae). with (CAMBEFORT,1991 b; SCHOLTZ & CHOW,19951, few representativestoday, such as Parentius, and to the Pleistocene habitat fragrnen- and Palaeonthophagus of the latigena tation (MONKONEN& WELSCH, 1994). group (MART~NPIERA & ZUNINO,1985). To test the idea that the lack of spe- Thus if the rnost specialized trophic cialist and true generalist dung beetle adaptations are confined to high-rank taxa fauna is either the result of pre-Neolithic (genera, subgenera and species groups), evolutionary events or Neolithic ecologic Palaearctic Region trophic structuring can changes in the Palaearctic Region, three be inferred to date, at the latest, frorn cornplernentary approachesare suggested; before appearance of the hurnan. two ecological and one phylogenetic. 1. If hurnan activity has favoured today's frequent and abundant species, through Conclusions sustained, intense rnodification of available trophic source type and frequency, 1. In the ternperate Palaearctic Region, dung beetle comrnunity structure changes trophic choice little influences Scarabaeoidea should be observed in areas nearly free of dung beetle cornmunity resource partition- hurnan influence. However, it will not be ing. Species are generally attracted to easy to find a site for testing this hypoth- hurnan and al1 types of herbivore faeces. esis, because of the lack of truly non-hu- Thus, polyphagy restricted to these kinds rnan-transformed ecosysterns in the West- of excrernents is the generalized condition. ern Palaearctic Region. Species segregation is generaily more 2. If the rich local Palaearctic dung beetle influenced by habitat than trophic cornrnunity's null (or nearly null) attrac- resource. tion toward carnivore and wild ornnivore 2. Both large- and srnall-population dung is the result of singular evolution- species are rnost attracted to hurnan and ary adaptations, rather than a response dornestic rnarnrnal faeces. There is no ex- to resource scarcity, then this trophic be- clusively wild herbivore faeces fauna, but haviour was probably a pre-Neolithic ad- rather an irnpoverished one, in cornparison aptation originated before those verte- with that of hurnan and dornestic ungu- brate populations decreased. late faeces. Carnivore faeces are hardly 3. Establishing trophic adaptation age: colonized at all. Polarizing the polyphagy-stenophagy in 3. The lengthy duration of the effects the prirnitive derived sense could be in- of the hurnan presence in the Palaearctic ferred frorn a reconstruction of the Region rnay explain why coprophagous phylogenetic relationships arnong species, Scarabaeoidea cornrnunity structure is nearly and rnapping on to the cladograrn one independent of trophic choice. However, or the other trophic pattern (BROOKS& the human irnpact alone, historically re- MCLENNAN,1991). A phylogenetic approach cent, does not explain the observed ab- Martín-Piera & Lobo sence of a true polyphagy in the regional Acknowledgements coprophagous Scarabaeoidea, extremely poor in communities that colonize car- The authors wish to thank Mn Milagro nivore and wild omnivore faeces. Coca (Museo Nacional de Ciencias Naturales; C.S.I.C.) and Alberto Donaire (Estación Biológica de Doñana, C.S.I.C.), Resumen for their help with the field work, and Domingo Iglesias Fuente, Research Discusión comparada sobre las preferen- granted student in the Museo Nacional cias tróficas en comunidades de escara- de Ciencias Naturales, 1992, for his as- bajos coprófagos sistance in laboratory and office. To Mr. James Cerne for his revision of different Se estudia la relevancia de la dimensión English drafts. trófica en el reparto de recursos, en una comunidad ibérica de escarabeidos coprófagos en el Parque Nacional de References Doñana. Se analizaron nueve clases diferentes de excrementos de vertebrados ANDUAGA,S. & HALFFTER,G., 1991. Escara- domésticos y salvajes (tabla 1). Los resul- bajos asociados a madrigueras de roe- tados indicaron que existe una atracción dores (Coleoptera: Scarabaeidae, indiferenciada a todo tipo de heces de Scarabaeinae). Folia Entomol. Mex., 81: herbívoros y deyecciones humanas (fig. 185-197. 1, tabla 2). Sin embargo, aunque la ÁVILA, J. M., SANDOVAL, P., SCHMIDT, J. & eurifagia en este tipo de heces es la con- SANCHEZ-PINERO,F., 1988. Contribución dición generalizada, los excrementos de al conocimiento de los Scarabaeoidea carnívoros y otros omnívoros, apenas son (Coleoptera) coprófagos de los excre- colonizados (fig. 2). No existe una fauna mentos de conejo de la provincia de exclusiva de las deyecciones de herbívo- Granada. (España). Elytron, 2: 41-50. ros salvajes. Se trata de una fauna empo- Bnz, A., 1988. Selección de macrohábitat brecida respecto a la que coloniza las heces por algunas especies y análisis de una humanas y las de ungulados domésticos comunidad de escarabeidos coprófagos (figs. 3-6). (Coleoptera) del macizo de Ayllón (Sis- Este patrón difiere del que se conoce tema Central, España). Annales de la en otras regiones biogeográficas. Se argu- Société Entomologique de france (N.S.), menta que la antigüedad de la transfor- 24: 203-210. mación antrópica en la Región Paleártica, BROOKS,D. R. & MACLENNAN.,D. A., 1991. puede explicar la escasa importancia de la Phylogeny, Ecology and Behaviour. A dimensión trófica en la estructura de es- research programme in Comparative tas comunidades. Sin embargo, la interven- Biology. University of Chicago Press, ción humana no acaba de explicar la au- Chicago. sencia de una verdadera polifagia, es de- CAMBEFORT,Y., 1991a. Dung beetles in cir, la colonización indiscriminada de todo tropical savannas. In: Dung Beetle Ecol- tipo de excrementos. ogy: 156-178 (1. Hanski &Y. Cambefort, Se sugieren algunas líneas de investiga- Eds.). Princeton University Press, New ción alternativas que permitirían evaluar Jersey. si la actual estructuración de las comuni- - 1991b. From saprophagy to coprophagy. dades coprófagas, respecto al factor recur- In: Dung Beetle Ecology: 22-35 (l. Hanski so, es un evento histórico reciente de ori- & Y. Cambefort, Eds.). Princeton Uni- gen antrópico o, por el contrario, se trata versity Press, New Jersey. de un evento preneolítico, cuyas causas CARPANETO,G. M. & FABBRI, M., 1983. Coleo- habrían de investigarse a escala evolutiva. tteri Scarabaeidae e Aphodiidae coprofagi Miscel.lania Zoologica 19.1 (1996)

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