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Heterotrophic succession within dung-inhabiting beetle communities in northern Spain
Acta Oecologica 20 (5) (1999) 527−535 / © 1999 Éditions scientifiques et médicales Elsevier SAS. All rights reserved.
Heterotrophic succession within dung-inhabiting beetle communities in northern Spain Rosa Menéndez *§, David Gutiérrez Departamento de Biología de Organismos y Sistemas, Unidad de Ecología, Universidad de Oviedo, Oviedo 33071, Spain. * Corresponding author (e-mail: [email protected])
Received January 30, 1999; revised June 1, 1999; accepted June 1, 1999
Abstract — Successional patterns of beetles inhabiting dung pats were examined during May and July 1993 in a mountain area in northern Spain (Picos de Europa). Beetles belonging to six families were caught during the course of succession (30 d). Coprophagous beetles were more abundant in dung pats than predatory beetles (89 and 11 %, respectively). A trophic sequence was observed in relation to age of the dung, coprophagous beetles occurring earlier in the dung than predatory beetles. The pattern was observed on two occasions during the season, though succession proceeded somewhat faster in July than in May. These results suggest that food availability and microclimatic conditions in dung pats appear to determine the successional occurrence of beetle taxa. On the other hand, coprophagous species (Aphodius) were poorly segregated along the successional axis. Null models failed to support the hypothesis that successional overlap and differences in successional mean occurrence between species could be the result of competition. Successional patterns at the specific level probably reflect differences in behaviour, such as pat location, feeding, mating, egg-laying and larva requirements, rather than competitive replacement. © 1999 Éditions scientifiques et médicales Elsevier SAS Competition / dung-inhabiting beetles / dung pats / food availability / heterotrophic succession / null model
1. INTRODUCTION The term heterotrophic succession is used to denote the serial change in species composition in ephemeral resource patches, such as dung pats, corpses, fruit and fungi, throughout the process of decomposition [21]. Several successional phases have been described for communities inhabiting dung pats [34, 42]. In the temperate zone, dung pats are frequently colonised first by fly species, followed by several beetle groups: coprophagous (Hydrophilidae, Scarabaeidae and Aphodiidae) and carnivorous (Histeridae, Staphylinidae and Carabidae). The last stages of decomposition are dominated by generalist species, such as earthworms, mites, nematodes and fungi, which are able to live in a wide range of habitats that contain decomposing organic matter. The energy sources available to animals in heterotrophic successions, in contrast to autotrophic suc§ Present address: Centre for Biodiversity & Conservation, School of Biology, University of Leeds, Leeds LS2 9JT, UK.
cessions, are largest at the beginning and decrease with time. As a result, most communities inhabiting ephemeral resource patches disappear after only one generation of colonists. Therefore, the successional processes in these heterotrophic systems are markedly different from those observed in autotrophic systems. Three mechanisms have been proposed to explain the course of most heterotrophic successions. (i) Succession involves a systematic change in species composition in relation to trophic requirements [8, 34]; for instance, as prey number increases in the dung pats, the abundance of predator species increases. Thus, the facilitation model of succession could be supported by dung pats, as many late arriving species seem to benefit from the activity and population growth of the early arrivals [6]. (ii) Successional patterns within guilds could be the result of competitive interactions between species. Interspecific competition appears to determine the course of succession in some heterotrophic systems [53], including some communities of dung beetles [9]. However, if competition is a major factor in structuring the successional process of temperate
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dung beetle assemblages, it has not been statistically tested ([8, 22, 30] but see [28] for beetle-fly interactions). (iii) Microclimatic conditions around the dung pats could determine the course of succession [22, 38]. Warm and dry weather rapidly decreases the moisture content of the dung pats, accelerating the successional process. A sound evaluation of the role of competition in structuring communities requires an experimental analysis. However, experimental studies on species competition are frequently restricted to a few species rather than the whole assemblage [13, 24, 49, 50]. The role of competition for a whole assemblage can be determined by examining the patterns of species cooccurrence [14, 45], or by using null models which involve the comparison of parameters between actual and randomly generated communities [5, 39, 43, 44, 47, 48, 52]. The aim of the present study is to determine how trophic requirements, seasonal conditions and competition affect successional patterns of beetle taxa inhabiting cattle dung in a mountain area located in the temperate zone. 2. MATERIALS AND METHODS 2.1. Study area and climatic conditions The study was conducted during May and July 1993 in Comeya (Asturias province, northern Spain, 43º17’ N, 4º59’ W), at 840 m above sea level, in a pasture (Merendero-Cynosuretum, see [51]) of about 200 ha, grazed by cattle, sheep and horses. Cattle droppings are the major source of dung for coprophagous beetles (recorded density of about 200 dung pats⋅ha–1, unpubl. data). Mean monthly temperature and monthly rainfall were, respectively, 9.1 °C and 129.5 mm in May, and 12.2 °C and 107.1 mm in July (La Picota Meteorological station, 1 100 m elevation). 2.2. Sampling Fresh cattle dung was collected, thoroughly mixed to homogenise the dung, and divided into a series of identical 1 000-g pats. Forty dung pats in each study month (May and July) were placed 3 m apart in five straight lines and eight columns. Five dung pats, one from each line and all from the same column, along with the 5-cm soil layer below the pat, were removed after 1, 2, 3, 4, 6, 10, 15 and 30 d in May, and after 1, 2, 3, 4, 6, 10, 15 and 25 d in July. Beetles were separated from the dung by submerging it in water and then collecting the animals rising to the surface. The beetles that had burrowed into the
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ground under the dung were also collected by handsorting the soil. Six beetle families inhabit dung pats in the study area: Hydrophilidae, Scarabaeidae, Aphodiidae, Staphylinidae, Histeridae and Carabidae. Scarabaeidae and Aphodiidae were identified to species (nomenclature follows Baraud [3]), while Hydrophilidae were identified to genera. 2.3. Data analysis As on some sampling occasions, a few dung pats were lost because of cattle damage; the catches of each taxonomic group and species were standardised to number of individuals per dung pat, except for calculating the successional mean occurrence of taxonomic groups (see below). The abundance matrices of taxonomic groups and species were analysed using detrended correspondence analysis (DCA). This is an indirect ordination method which simultaneously ordinates samples and species [12]. DCA is appropriate for long gradients in which species abundance is a unimodal function of position along the gradient [54]. Eigenvalues associated with each axis of DCA ordination equal the degree of correlation (r2) between species and sampling scores [12, 46]. DCA scores were plotted on bidimensional diagrams, and interpretations of axes were made on the basis of both visual inspection of the bidimensional plots and simple regression of sample scores against environmental variables [54]. Successional patterns were described by the successional mean occurrence (SMO), which is the average of the colonisation curve expressed in days [19]. The formula for the calculation of SMO is: n
( p~t − t i
SMO =
i
i − 1 ! ti
i
n
( p~t − t i
i
i − 1!
i
where pi is the number of individuals extracted from droppings of age ti (in days), and n the number of ‘sampling points’ along the succession. The abundance of taxonomic groups was measured separately for each dung pat. The eight pats which were exposed in one line were used to calculate one SMO value, which allowed the calculation of five SMO values for each month. SMO values were also calculated separately for each Aphodius species. In this case, the number of Aphodius extracted from five pats of the same age had to be averaged due to low sample sizes. Therefore, only one SMO value per Aphodius species per month was calculated. In addition, the successional patterns of Aphodius species were studied using two other parameters: Acta Oecologica
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Heterotrophic succession in dung beetles
– Successional width (SD), as a measure of the time spent within a dung pat, and calculated as the standard deviation of the successional mean occurrence. – Successional overlap between pairs of species (PS), measured as the percentage similarity [18], which may be written as:
PSjk = 1 −
S21 ( u p n
jn
− pkn u
D
where pjn and pkn are the proportions of individuals of species j and k associated with pat age n. Pat age categories were eight for May, but only six for July, because in this case, there were no individuals in the dung pats aged 15 and 25 d. For each month, the mean successional overlap was calculated as the average of the overlaps between all pair-wise combinations of species. 2.4. Null model Successional segregation of Aphodius species was analysed using null model tests for competitive displacement. Null models involve comparisons of species’ relationships in an observed community with those of randomly constructed communities [47]. SMO values and mean PS were used to test successional segregation against the null hypothesis that both parameters were taken from a random distribution. In both cases, the procedure to test competitive displacement involved the random placement on the resource axis (successional axis) of SMO values or successional curves of all species in the community. Two aspects are important when testing competitive displacement in resource use within communities; that all species use the same resource [7, 48] and that the resource is uniformly distributed over time [26]. Tests were performed for all Aphodius species in each study month, ten species for May and nine for July. Axis endpoint was the maximum number of days for which at least one individual was caught (30 d for May and 10 d for July), assuming that resources were uniformly available over the period in which at least one individual beetle was found in dung. The procedure for testing SMO evenness involved the calculation of the distances (in days) between all pairs of consecutive SMO values, and the calculation from these distances of the shortest one (MIN) and their variance (VAR). The use of several parameters when testing competitive displacement is required because single tests fail to detect displacement in some cases. For instance, the presence of an outlier in an otherwise highly organised community is correctly evaluated by analysing MIN, while tests based on VAR are effective in detecting displacement in a community structured by competition in which only one species breaks the pattern (for further details, see [1]). Vol. 20 (5) 1999
Following the same procedure, MIN and VAR were calculated based upon randomly and independently placed continuous SMO values on the successional axis, the number of random SMO values being the same as the species number within the actual community. This procedure was iterated 3 000 times by a Turbo Pascal subroutine (a minimum of 2 000 iterations is suggested [41]). Finally, the probability of the randomly generated SMO values being more spaced out than the observed values was determined by the ratio between the number of iterations showing higher MIN values and lower VAR values than observed values, and the total number of iterations. The null hypothesis was rejected if those probabilities were lower than 0.05. The successional segregation of species was also analysed by comparing the overlap between all species pairs of the actual assemblage with those of randomly generated assemblages [39, 47]. In random assemblages, the shape of the successional curve for each species remained the same as observed while their position changed. The whole successional curve of all species was simply relocated by chance to another point along the dung pat age axis. This procedure was iterated 3 000 times by a Turbo Pascal subroutine. The probability that randomly generated assemblages show a mean successional overlap lower than the actual assemblage was the ratio between the number of iterations with overlap values lower than the observed ones, and the total number of iterations. 3. RESULTS A total of 2 403 beetles inhabiting cattle dung belonging to six families was caught during the sampling period. Coprophagous beetles were numerically dominant in dung pats: Hydrophilidae (gr. Cercyon 40.5 % and Sphaeridium 19.5 %), Aphodiidae (24 %) and Scarabaeidae (5 %). Amongst the predatory beetles, Staphylinidae was the most abundant family comprising approximately 10 % of catches, while Histeridae and Carabidae abundance made up 0.3 and 0.2 % of catches, respectively. 3.1. Successional patterns of taxonomic groups Data analyses were restricted to the four most abundant beetle families. The successional pattern of Hydrophilidae was analysed separately for the genera Sphaeridium and Cercyon. Figure 1 shows the relative abundance of five beetle groups in dung pats of different age. Most individuals occurred in dung during the first 5 d following deposition. Eigenvalues for the first and second DCA axis on the abundance matrix were 0.238 and 0.126. Axis 1
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R. Menéndez, D. Gutiérrez
Figure 1. Successional variation in the number of individuals of five beetle taxa inhabiting dung pats (— May and ---- July). M, Sample size in May; J, sample size in July.
was interpreted as pat age since samples were ordinated along the first axis in increasing pat age (r2 = 0.61, F = 20.32, df = 1, 13, P < 0.001, figure 2). Moreover, pats of a given age in July tended to show lower axis 1 scores than those in May. Axis 2 was not associated either with pat age or with months. According to the interpretation of axis 1, there was a taxonomic replacement throughout the successional process. Sphaeridium and Cercyon were associated with fresh pats, Scarabaeidae with mid-age pats and Aphodiidae and Staphylinidae with old pats. Successional mean occurrence values (SMO) were higher in May than in July for all beetle groups (table I). SMO in May was positively correlated with SMO in July (r = 0.96, n = 5, P = 0.003). Sphaeridium showed the lowest SMO values because average abundance occurred on the first days of the succession; in contrast, the late occurrence of Aphodiidae and Staphylinidae is shown by their higher SMO values.
Figure 2. Ordination of sampling pats varying in age (d, May; s, July) (a), and beetle taxa (b) by detrended correspondence analysis. The ordination space is identical in both figures. The number next to each symbol is the age of the pat in days (a). (b) Names of the beetle taxa (Sphae, Sphaeridium; Cercy, Cercyon; Scara, Scarabaeidae; Aphod, Aphodiidae; Staph, Staphylinidae).
3.2. Successional patterns of coprophagous species A total of 581 dung beetles belonging to twelve Aphodius species were caught. Except A. obscurus, all species arrived on the pats during the first 3 d (table II). Eigenvalues for the first and second DCA axis Acta Oecologica
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Heterotrophic succession in dung beetles
Table I. Successional mean occurrence (SMO) in days for five beetle groups recorded in two sampling months. Values are given as mean ± 1 SD, with sample sizes in brackets. Statistical significance of ANOVA (F) and Mann-Whitney (U) tests are shown in the last column. * Log-transformed data. Taxa Hydrophilidae: Sphaeridium Cercyon Scarabaeidae Aphodiidae Staphylinidae
May
July
2.7 ± 0.4 (5) 4.1 ± 0.3 (5) 4.1 ± 1.4 (5) 10.0 ± 1.6 (5) 8.7 ± 1.6 (5)
1.8 ± 0.1 (5) 2.5 ± 0.3 (5) 3.0 ± 0.1 (5) 4.3 ± 0.3 (5) 4.5 ± 0.5 (5)
F* = 4.64, P = 0.06 F = 13.90, P = 0.006 U = 16, P > 0.2 F* = 20.38, P = 0.002 F* = 7.30, P = 0.03
Table II. First date of occurrence and successional mean occurrence (SMO) in days for all Aphodius species recorded in two sampling months. Species
A. prodromus A. erraticus A. fimetarius A. conspurcatus A. pusillus A. depressus A. haemorrhoidalis A. fossor A. obscurus A. ater A. scybalarius A. rufipes
May SMO
n
1 3 2 3 1 1 1 1 10 1
2.11 3.00 3.00 3.00 4.09 8.44 8.90 11.97 12.43 13.67
2 2 2 1 184 10 15 3 2 133
were, respectively, 0.372 and 0.197. Neither axis 1 nor axis 2 was correlated with dung pat age (P > 0.5). SMO values in May were not correlated with SMO values in July (r = –0.17, n = 7, P = 0.716). On other hand, the successional widths (SD) of Aphodius species were positively correlated to successional mean occurrence (SMO) both in May (r = 0.80, n = 9, P = 0.009) and in July (r = 0.93, n = 8, P = 0.001). SMO values of Aphodius species ranged from 2.11 to 13.67 in May and from 1 to 7.95 in July (table II). However, this did not imply a significantly more even distribution than expected at random (table III). The probability that a randomly generated community showed parameters more evenly distributed than the actual assemblage was higher than 0.05 in most cases. VAR value in May was the only statistically significant comparison. Likewise, mean successional overlap (PS) was 0.299 in May and 0.392 in July. These values were not Vol. 20 (5) 1999
July
First date
First date
SMO
n
1 2
1.00 7.95
2 10
1 1 2 2
3.86 2.00 5.64 3.11
53 25 51 9
1 2 2
3.49 2.50 3.00
72 2 3
significantly lower than those randomly expected (P = 0.851 in May and P = 0.916 in July). 4. DISCUSSION The results presented here show that there was a faunal turnover of beetles inhabiting dung pats in Table III. One-tailed P-level probabilities for minimum (MIN) and variance (VAR) of SMO differences between Aphodius species for the whole assemblages in May (30-d axis) and July (10-d axis). Probabilities are the ratio between the number of random iterations showing higher MIN values, and lower VAR values than observed values, and the total number of iterations (3 000 random assemblages for each sampling month). Parameters
MIN VAR
Observed values
Probabilities
May
July
May
July
0.000 2.180
0.110 0.609
1.000 0.036*
0.391 0.423
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relation to age of dung. A taxonomic sequence was observed throughout the process of dung decomposition: Hydrophilidae (Sphaeridium and Cercyon), Scarabaeidae, Aphodiidae and Staphylinidae. The same taxonomic sequence was observed on two occasions during the season, though succession proceeded somewhat faster in July than in May. This fact may be attributable to different weather conditions over the season [19, 36, 37]. Temperature increases the bacterial activity and the loss in moisture content in dung pats, leading to an accelerated successional process [22, 35, 38]. Similar successional patterns have been found for dung beetle assemblages in other temperate regions [11, 32, 34, 36]. Differences in successional occurrence between groups have been attributed to differences in food requirements and resource availability [8, 34]. Dung pats are maximally distinct from their surroundings at the moment of their origin and guilds of specialist species are the first colonisers, while soil generalist and predator species progressively colonise the dung pats as they become more similar to their surroundings [21]. Carnivorous beetles seem to be largely dependent on the number of suitable preys in droppings. The main food of Staphylinidae species consists of larvae of flies and dung beetles, which are not available during the first days of succession [34]. Dung beetle larvae in dung pats consume dung in a seemingly unselective manner [29] while adults typically use dung juices [22, 23, 35]. A dung pat represents a highly concentrated parcel of energy, but it contains resources which disappear under the effects of microbial activity and physical factors [31]. Competition could be severe in ephemeral habitats because the nutrient availability is maximum at the beginning, subsequently decreasing with time. A strategy of arriving in the dropping as early as possible could be advantageous for specialist coprophagous that are able to ensure a portion of the resource for exclusive use, but not for species that stay and potentially compete for a prolonged period of time [22, 25]. This hypothesis could explain the differences between SMO of Scarabaeidae and Aphodiidae, since these taxa show contrasting breeding behaviours. In most cases, Scarabaeidae species do not feed within dung pats, but are nesting beetles which dig a vertical tunnel under or outside the pat and then transport dung to the bottom of the burrow [17]. Thus, a portion of the resource is protected against competitors and climatic conditions, and may be used for both larval and adult feeding [4]. An early arrival in dung
R. Menéndez, D. Gutiérrez
pats could provide a crucial advantage for nesters because they are able to remove rapidly a portion of resource for their exclusive use [22]. Nevertheless, only one species (Onthophagus similis) accounted for 98 % of Scarabaeidae caught, hence the successional patterns observed for Scarabaeidae as a whole might be largely determined by the requirements of that species. In contrast, the larval development and adult feeding of most Aphodius species take place within dung pats [4], and therefore, they are not able to monopolise a portion of dung. In this case, a successional segregation in resource use could be expected. However, results from the null models gave no evidence of such successional segregation of Aphodius species, not supporting competition as a possible explanation for the differences in successional occurrence of species [30]. Our results on competition in Aphodius species were based on the outcome of null models. Even random models are based upon a number of assumptions which will determine their predictions. Though some assumptions are implicit in all tests of niche differentiation and can only be regarded as an inevitable approximation (see [48] for a discussion), others have considerable effects on the outcome of the tests and must be discussed in order to understand the limitations when applying the model [39]. First, a critical decision is how to define the important interacting species to be considered in the analysis. To test competitive displacement obviously only species that constitute a guild, as those sharing a resource, should be included [7, 48]. Thus, Aphodius species were treated as a single guild at least when considering potential interactions among adults, given the similarity of adult feeding methods [4]. However, dominant species could show greater niche complementariness than the whole community [39], and significant niche differences between dominant species could not be detected if all coprophagous species are considered. We performed additional analyses including only the four most abundant species in each month, but they produced similar results to those for the whole assemblage (table IV). The values of mean successional overlap for this subset were not significantly lower than those randomly expected either (P > 0.05). Second, a uniform distribution of resource must be assumed when testing competitive displacement in resource use within communities [26]. Nutritional requirements of Aphodius species are insufficiently known; although adult beetles obtain all or most of their nutrition from dung juices, the specific comActa Oecologica
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Table IV. One-tailed P-level probabilities for minimum (MIN) and variance (VAR) of SMO differences between Aphodius species for subsets of the whole assemblages in May and July. Probabilities as in table III. Parameters
All species, 10-d axis MIN VAR Four abundant species, 30-d axis MIN VAR Four abundant species, 10-d axis MIN VAR
Observed values
Probabilities
May
July
May
July
0.000 0.615
– –
1.000 0.383
– –
0.460 5.647
– –
0.863 0.138
– –
0.694 0.657
0.370 1.005
0.375 0.273
1.000 0.091
pounds used have not been studied [2, 22]. Adult resource availability seems to be dependent on the water content in the dung, and dung containing moisture values lower than 68 % could be unsuitable for some coprophagous species [10]. The water content in a dung pat decreases relatively slowly during the first 10 d and moisture values are frequently higher than 75 % during this time period [16, 31]. Given the difficulty of clearly defining the availability of resources in the pat, we performed additional null model tests using an endpoint of 10 d in May, which assumes that the chemical composition of resources was relatively constant during that period. These analyses, however, produced no significant results either for successional mean occurrence (table IV) or for mean successional overlap (P > 0.05). Our results of the null model tests were not significant for most cases, and both the set of species selected and the time scale considered had no effect on the outcome of the tests. Although non-significant results do not mean that the alternative hypothesis must be rejected, it seems unlikely that interspecific differences in adult successional occurrence have been the result of past or present competition interactions. Competition might not be a major factor if the resource is not limited. Holter [30] showed that the Aphodius guild inhabiting a dung pat requires only a negligible fraction (0.3 %) of the initial energy in the dung. On the other hand, interspecific differences in SMO were not consistent between sampling months and there was no clear species turnover over the successional process. This was not in agreement with Gittings and Giller [16] who found a successional species turnover of Aphodius species over dung pat decomposition. In our study, dung pat age did not Vol. 20 (5) 1999
determine species composition because most of the species were present in the dung pat during the first 10 d, and only a few was present in old pats. Differences in SMO between species could be simply the result of differences in residence time within dung pats [20]; this explanation was supported by the positive relationship between successional mean occurrence and standard deviation. Most species arrive early on the pats (first and second days, see table II), but some species stay longer in a given dropping than others. It is difficult to identify the main reason for these differences. Fresh dung pats could attract more beetles than old pats because coprophagous beetles use their olfactory senses to locate dung pats [35, 40]. Thus, adults mainly colonise fresh dung pats and leave them when the drying of dung makes it unsuitable as food [33]. However, adult activity in the pats could reflect other requirements, such as mating, egg-laying, or larval feeding [20]. For instance, immature females of A. ater tended to occur in fresher pats than mature females, because females colonised fresh pats and matured reproductively within them [27]. Moreover, Aphodius species differ in oviposition behaviour and these differences may be important in determining species succession [15, 16]. Early successional species lay their eggs in the soil because wet dung is not suitable for eggs and larval survival, while mid and late species lay their eggs in dung. Though oviposition behaviour was not known for all species included in the present study, our results seem to be relatively consistent with that hypothesis. Thus, soilovipositing species (e.g. A. prodromus, A. erraticus, A. rufipes) showed smaller SMO than dung-ovipositing species (A. fimetarius, A. fossor, A. ater).
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The present results suggest that the facilitation model of succession [6] is supported by the successional process in dung pats, as many late-arriving species seem to benefit from the activity and population growth of the early arrivals. The food availability and microclimatic conditions around dung seem to determine the successional occurrence of beetle taxa. In dung beetle succession, interspecific competition is not likely to occur among adults because beetle density is low relative to resource supply. The drying of dung may be the decisive factor in determining pat colonisation by coprophagous species, while the residence time in the pat could reflect other specific requirements (mating, egg-laying and larva feeding requirements). Acknowledgments We thank Marcos Méndez for assistance with the field work and Silvino Menéndez for carrying out the Turbo Pascal subroutines. Robert J. Wilson kindly improved the English. José R. Obeso and two anonymous referees provided useful criticism on an earlier version of the manuscript. A. M. Felicísimo kindly provided climatic data. The Instituto para la Conservación de la Naturaleza (ICONA) provided funds, climatic data and permission for trapping beetles in the Picos de Europa National Park.
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[9] Doube B.M., Giller P.S., Moola F., Dung burial strategies in some South African coprine and onitine dung beetles (Scarabaeidae, Scarabaeinae), Ecol. Entomol. 13 (1988) 251–261. [10] Edwards P.B., Seasonal variation in the dung of African grazing mammals, and its consequences for coprophagous, Funct. Ecol. 5 (1991) 617–628. [11] Franch J., Domènech J., Sánchez C., La successió d’invertebrats en les buines de vaquí a la vall d’Aisa (Pirineu aragonès), Orsis 5 (1990) 113–134. [12] Gauch Jr H.G., Multivariate Analysis in Community Ecology, Cambridge University Press, Cambridge, 1982. [13] Giller P.S., Doube B.M., Experimental analysis of inter- and intraspecific competition in dung beetle communities, J. Anim. Ecol. 58 (1989) 129–142. [14] Giller P.S., Doube B.M., Spatial and temporal co-occurrence of competitors in Southern African dung beetle communities, J. Anim. Ecol. 63 (1994) 629–643. [15] Gittings T., Giller P.S., Life history traits and resource utilisation in an assemblage of north temperate Aphodius dung beetles (Coleoptera: Scarabaeidae), Ecography 20 (1997) 55–66. [16] Gittings T., Giller P.S., Resource quality and the colonisation and succession of coprophagous dung beetles, Ecography 21 (1998) 581–592. [17] Halffter G., Edmonds W.D., The nesting behavior of dung beetles (Scarabaeinae): an ecological and evolutive approach, Instituto de Ecología, México, 1982. [18] Hanski I., Some comments on the measurement of niche metrics, Ecology 59 (1978) 168–174. [19] Hanski I., Patterns of beetle succession in droppings, Ann. Zool. Fenn. 17 (1980) 17–25. [20] Hanski I., Migration to and from cow droppings by coprophagous beetles, Ann. Zool. Fenn. 17 (1980) 11–25. [21] Hanski I., Colonization of ephemeral habitats, in: Gray A.J., Crawley M.J., Edwards P.J. (Eds.), Colonization, Succession and Stability, Blackwell Scientific Publications, Oxford, 1987, pp. 155–185. [22] Hanski I., Nutritional ecology of dung- and carrion-feeding insects, in: Slansky Jr F., Rodríguez J.G. (Eds.), Nutritional Ecology of Insects, Mites and Spiders, Wiley, New York, 1987 pp. 837–884. [23] Hanski I., The dung insect community, in: Hanski I., Cambefort Y. (Eds.), Dung Beetle Ecology, Princeton University Press, Princeton, 1991, pp. 5–21. [24] Hanski I., Cambefort Y., Competition in dung beetles, in: Hanski I., Cambefort Y. (Eds.), Dung Beetle Ecology, Princeton University Press, Princeton, 1991, pp. 305–329. [25] Hanski I., Koskela H., Niche relations amongst dunginhabiting beetles, Oecologia 28 (1977) 203–231. [26] Harvey P.H., Colwell R.K., Silvertown J.W., May R.M., Null models in ecology, Annu. Rev. Ecol. Syst. 14 (1983) 189–211. [27] Hirschberger P., Spatial distribution, resource utilisation and intraspecific competition in the dung beetle Aphodius ater, Oecologia 116 (1998) 136–142. [28] Hirschberger P., Degro H.N., Oviposition of the dung beetle Aphodius ater in relation to the abundance of yellow dungfly larvae (Scatophaga stercoraria), Ecol. Entomol. 21 (1996) 352–357. [29] Holter P., Food utilization of dung-eating Aphodius larvae (Scarabaeidae), Oikos 25 (1974) 71–79. [30] Holter P., Resource utilization and local coexistence in a guild of scarabaeid dung beetles (Aphodius spp.), Oikos 39 (1982) 213–227. Acta Oecologica
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[31] Holter P., Concentration of oxygen, carbon dioxide and methane in the air within dung pats, Pedobiologia 35 (1991) 381–386. [32] Kessler H., Balshaugh E.U., Succession of adult coleoptera in bovine manure in east central south Dakota, Ann. Entomol. Soc. Am. 65 (1972) 1333–1336. [33] Koskela H., Habitat selection of dung-inhabiting Staphylinids (Coleoptera) in relation to age of the dung, Ann. Zool. Fenn. 9 (1972) 156–171. [34] Koskela H., Hanski I., Structure and succession in a beetle community inhabiting cow dung, Ann. Zool. Fenn. 14 (1977) 204–223. [35] Landin B.O., Ecological studies on dung-beetles, Opusc. Entomol. 19 (Suppl.) (1961) 1–227. [36] Lobo J.M., Microsucesión de insectos en heces de vacuno: influencia de las condiciones ambientales y relación entre grupos tróficos, Graellsia 48 (1992) 71–85. [37] Lobo J.M., El relevo microsucesional entre los Scarabaeoidea coprófagos (Col.), Misc. Zool. 16 (1992) 45–59. [38] Lobo J.M., Veiga C.M., Interés ecológico y económico de la fauna coprófaga en pastos de uso ganadero, Ecología 4 (1990) 313–331. [39] Loreau M., On testing temporal niche differentiation in carabid beetles, Oecologia 81 (1989) 89–96. [40] Lumaret, J.P., Galante E., Lumbreras C., Mena J., Bertrand M., BerBernal J.L., Cooper J.F., Kadiri N., Crowe D., Field effects of ivermectin residues on dung beetles, J. Appl. Ecol. 30 (1993) 428–436 . [41] Manly B.F.I., Randomization and Monte Carlo Methods in Biology, Chapman & Hall, London, 1991. [42] Mohr C.O., Cattle droppings as ecological units, Ecol. Monogr. 13 (1943) 275–298. [43] Niemelä J., Interspecific competition in ground-beetle assemblages (Carabidae): what have we learned?, Oikos 66 (1993) 325–335.
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535 [44] Palmer M., Testing for seasonal displacement in a dung beetle guild, Ecography 18 (1995) 173–177. [45] Peck S.B., Forsyth A., Composition, structure and competitive behaviour in a guild of Ecuadorian rain forest dung beetles (Coleoptera: Scarabaeidae), Can. J. Zool. 60 (1982) 1624–1634. [46] Pielou E.C., The interpretation of ecological data: a primer on classification and ordination, John Wiley & Sons, New York, 1984. [47] Pleasants J.M., Null-model tests for competitive displacement: the fallacy of not focusing on the whole community, Ecology 71 (1990) 1078–1084. [48] Rathcke B.J., Patterns of flowering phenologies: testability and causal inference using a random model, in: Strong Jr D.R., Simberloff D., Abele L.G., Thistle A.B. (Eds.), Ecological Communities: Conceptual Issues and the Evidence, Princeton University Press, Princeton, 1984, pp. 383–396. [49] Ridsdill-Smith T.J., Competition in dung breeding insects, in: Bailey W.J., Ridsdill-Smith T.J. (Eds.), Reproductive Behaviour in Insects-Individuals and Populations, Chapman & Hall, London, 1990, pp. 264–292. [50] Ridsdill-Smith T.J., Asymmetric competition in cattle dung between two species of Onthophagus dung beetle and the bush fly, Musca vetustissima, Ecol. Entomol. 18 (1993) 241–246. [51] Rivas-Martínez S., Díaz T.E., Fernández J.A., Loidi J., Penas A., La Vegetación de la Alta Montaña Cantábrica. Los Picos de Europa, Ediciones Leonesas, León, 1984. [52] Simberloff D., Boecklen W., Santa Rosalia reconsidered: size ratios and competition, Evolution 35 (1981) 1206–1228. [53] Swift M.J., Organization of assemblages of decomposer fungi in space and time, in: Gee J.H.R., Giller P.S. (Eds.), Organization of Communities: Past and Present, Blackwell Scientific Publications, Oxford, 1987, pp. 229–253. [54] TerBraak C.J.F., Prentice I.C., A theory of gradient analysis, Adv. Ecol. Res. 18 (1988) 271–317.
Heterotrophic succession within dung-inhabiting beetle communities in northern Spain Rosa Menéndez *§, David Gutiérrez Departamento de Biología de Organismos y Sistemas, Unidad de Ecología, Universidad de Oviedo, Oviedo 33071, Spain. * Corresponding author (e-mail: [email protected])
Received January 30, 1999; revised June 1, 1999; accepted June 1, 1999
Abstract — Successional patterns of beetles inhabiting dung pats were examined during May and July 1993 in a mountain area in northern Spain (Picos de Europa). Beetles belonging to six families were caught during the course of succession (30 d). Coprophagous beetles were more abundant in dung pats than predatory beetles (89 and 11 %, respectively). A trophic sequence was observed in relation to age of the dung, coprophagous beetles occurring earlier in the dung than predatory beetles. The pattern was observed on two occasions during the season, though succession proceeded somewhat faster in July than in May. These results suggest that food availability and microclimatic conditions in dung pats appear to determine the successional occurrence of beetle taxa. On the other hand, coprophagous species (Aphodius) were poorly segregated along the successional axis. Null models failed to support the hypothesis that successional overlap and differences in successional mean occurrence between species could be the result of competition. Successional patterns at the specific level probably reflect differences in behaviour, such as pat location, feeding, mating, egg-laying and larva requirements, rather than competitive replacement. © 1999 Éditions scientifiques et médicales Elsevier SAS Competition / dung-inhabiting beetles / dung pats / food availability / heterotrophic succession / null model
1. INTRODUCTION The term heterotrophic succession is used to denote the serial change in species composition in ephemeral resource patches, such as dung pats, corpses, fruit and fungi, throughout the process of decomposition [21]. Several successional phases have been described for communities inhabiting dung pats [34, 42]. In the temperate zone, dung pats are frequently colonised first by fly species, followed by several beetle groups: coprophagous (Hydrophilidae, Scarabaeidae and Aphodiidae) and carnivorous (Histeridae, Staphylinidae and Carabidae). The last stages of decomposition are dominated by generalist species, such as earthworms, mites, nematodes and fungi, which are able to live in a wide range of habitats that contain decomposing organic matter. The energy sources available to animals in heterotrophic successions, in contrast to autotrophic suc§ Present address: Centre for Biodiversity & Conservation, School of Biology, University of Leeds, Leeds LS2 9JT, UK.
cessions, are largest at the beginning and decrease with time. As a result, most communities inhabiting ephemeral resource patches disappear after only one generation of colonists. Therefore, the successional processes in these heterotrophic systems are markedly different from those observed in autotrophic systems. Three mechanisms have been proposed to explain the course of most heterotrophic successions. (i) Succession involves a systematic change in species composition in relation to trophic requirements [8, 34]; for instance, as prey number increases in the dung pats, the abundance of predator species increases. Thus, the facilitation model of succession could be supported by dung pats, as many late arriving species seem to benefit from the activity and population growth of the early arrivals [6]. (ii) Successional patterns within guilds could be the result of competitive interactions between species. Interspecific competition appears to determine the course of succession in some heterotrophic systems [53], including some communities of dung beetles [9]. However, if competition is a major factor in structuring the successional process of temperate
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dung beetle assemblages, it has not been statistically tested ([8, 22, 30] but see [28] for beetle-fly interactions). (iii) Microclimatic conditions around the dung pats could determine the course of succession [22, 38]. Warm and dry weather rapidly decreases the moisture content of the dung pats, accelerating the successional process. A sound evaluation of the role of competition in structuring communities requires an experimental analysis. However, experimental studies on species competition are frequently restricted to a few species rather than the whole assemblage [13, 24, 49, 50]. The role of competition for a whole assemblage can be determined by examining the patterns of species cooccurrence [14, 45], or by using null models which involve the comparison of parameters between actual and randomly generated communities [5, 39, 43, 44, 47, 48, 52]. The aim of the present study is to determine how trophic requirements, seasonal conditions and competition affect successional patterns of beetle taxa inhabiting cattle dung in a mountain area located in the temperate zone. 2. MATERIALS AND METHODS 2.1. Study area and climatic conditions The study was conducted during May and July 1993 in Comeya (Asturias province, northern Spain, 43º17’ N, 4º59’ W), at 840 m above sea level, in a pasture (Merendero-Cynosuretum, see [51]) of about 200 ha, grazed by cattle, sheep and horses. Cattle droppings are the major source of dung for coprophagous beetles (recorded density of about 200 dung pats⋅ha–1, unpubl. data). Mean monthly temperature and monthly rainfall were, respectively, 9.1 °C and 129.5 mm in May, and 12.2 °C and 107.1 mm in July (La Picota Meteorological station, 1 100 m elevation). 2.2. Sampling Fresh cattle dung was collected, thoroughly mixed to homogenise the dung, and divided into a series of identical 1 000-g pats. Forty dung pats in each study month (May and July) were placed 3 m apart in five straight lines and eight columns. Five dung pats, one from each line and all from the same column, along with the 5-cm soil layer below the pat, were removed after 1, 2, 3, 4, 6, 10, 15 and 30 d in May, and after 1, 2, 3, 4, 6, 10, 15 and 25 d in July. Beetles were separated from the dung by submerging it in water and then collecting the animals rising to the surface. The beetles that had burrowed into the
R. Menéndez, D. Gutiérrez
ground under the dung were also collected by handsorting the soil. Six beetle families inhabit dung pats in the study area: Hydrophilidae, Scarabaeidae, Aphodiidae, Staphylinidae, Histeridae and Carabidae. Scarabaeidae and Aphodiidae were identified to species (nomenclature follows Baraud [3]), while Hydrophilidae were identified to genera. 2.3. Data analysis As on some sampling occasions, a few dung pats were lost because of cattle damage; the catches of each taxonomic group and species were standardised to number of individuals per dung pat, except for calculating the successional mean occurrence of taxonomic groups (see below). The abundance matrices of taxonomic groups and species were analysed using detrended correspondence analysis (DCA). This is an indirect ordination method which simultaneously ordinates samples and species [12]. DCA is appropriate for long gradients in which species abundance is a unimodal function of position along the gradient [54]. Eigenvalues associated with each axis of DCA ordination equal the degree of correlation (r2) between species and sampling scores [12, 46]. DCA scores were plotted on bidimensional diagrams, and interpretations of axes were made on the basis of both visual inspection of the bidimensional plots and simple regression of sample scores against environmental variables [54]. Successional patterns were described by the successional mean occurrence (SMO), which is the average of the colonisation curve expressed in days [19]. The formula for the calculation of SMO is: n
( p~t − t i
SMO =
i
i − 1 ! ti
i
n
( p~t − t i
i
i − 1!
i
where pi is the number of individuals extracted from droppings of age ti (in days), and n the number of ‘sampling points’ along the succession. The abundance of taxonomic groups was measured separately for each dung pat. The eight pats which were exposed in one line were used to calculate one SMO value, which allowed the calculation of five SMO values for each month. SMO values were also calculated separately for each Aphodius species. In this case, the number of Aphodius extracted from five pats of the same age had to be averaged due to low sample sizes. Therefore, only one SMO value per Aphodius species per month was calculated. In addition, the successional patterns of Aphodius species were studied using two other parameters: Acta Oecologica
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– Successional width (SD), as a measure of the time spent within a dung pat, and calculated as the standard deviation of the successional mean occurrence. – Successional overlap between pairs of species (PS), measured as the percentage similarity [18], which may be written as:
PSjk = 1 −
S21 ( u p n
jn
− pkn u
D
where pjn and pkn are the proportions of individuals of species j and k associated with pat age n. Pat age categories were eight for May, but only six for July, because in this case, there were no individuals in the dung pats aged 15 and 25 d. For each month, the mean successional overlap was calculated as the average of the overlaps between all pair-wise combinations of species. 2.4. Null model Successional segregation of Aphodius species was analysed using null model tests for competitive displacement. Null models involve comparisons of species’ relationships in an observed community with those of randomly constructed communities [47]. SMO values and mean PS were used to test successional segregation against the null hypothesis that both parameters were taken from a random distribution. In both cases, the procedure to test competitive displacement involved the random placement on the resource axis (successional axis) of SMO values or successional curves of all species in the community. Two aspects are important when testing competitive displacement in resource use within communities; that all species use the same resource [7, 48] and that the resource is uniformly distributed over time [26]. Tests were performed for all Aphodius species in each study month, ten species for May and nine for July. Axis endpoint was the maximum number of days for which at least one individual was caught (30 d for May and 10 d for July), assuming that resources were uniformly available over the period in which at least one individual beetle was found in dung. The procedure for testing SMO evenness involved the calculation of the distances (in days) between all pairs of consecutive SMO values, and the calculation from these distances of the shortest one (MIN) and their variance (VAR). The use of several parameters when testing competitive displacement is required because single tests fail to detect displacement in some cases. For instance, the presence of an outlier in an otherwise highly organised community is correctly evaluated by analysing MIN, while tests based on VAR are effective in detecting displacement in a community structured by competition in which only one species breaks the pattern (for further details, see [1]). Vol. 20 (5) 1999
Following the same procedure, MIN and VAR were calculated based upon randomly and independently placed continuous SMO values on the successional axis, the number of random SMO values being the same as the species number within the actual community. This procedure was iterated 3 000 times by a Turbo Pascal subroutine (a minimum of 2 000 iterations is suggested [41]). Finally, the probability of the randomly generated SMO values being more spaced out than the observed values was determined by the ratio between the number of iterations showing higher MIN values and lower VAR values than observed values, and the total number of iterations. The null hypothesis was rejected if those probabilities were lower than 0.05. The successional segregation of species was also analysed by comparing the overlap between all species pairs of the actual assemblage with those of randomly generated assemblages [39, 47]. In random assemblages, the shape of the successional curve for each species remained the same as observed while their position changed. The whole successional curve of all species was simply relocated by chance to another point along the dung pat age axis. This procedure was iterated 3 000 times by a Turbo Pascal subroutine. The probability that randomly generated assemblages show a mean successional overlap lower than the actual assemblage was the ratio between the number of iterations with overlap values lower than the observed ones, and the total number of iterations. 3. RESULTS A total of 2 403 beetles inhabiting cattle dung belonging to six families was caught during the sampling period. Coprophagous beetles were numerically dominant in dung pats: Hydrophilidae (gr. Cercyon 40.5 % and Sphaeridium 19.5 %), Aphodiidae (24 %) and Scarabaeidae (5 %). Amongst the predatory beetles, Staphylinidae was the most abundant family comprising approximately 10 % of catches, while Histeridae and Carabidae abundance made up 0.3 and 0.2 % of catches, respectively. 3.1. Successional patterns of taxonomic groups Data analyses were restricted to the four most abundant beetle families. The successional pattern of Hydrophilidae was analysed separately for the genera Sphaeridium and Cercyon. Figure 1 shows the relative abundance of five beetle groups in dung pats of different age. Most individuals occurred in dung during the first 5 d following deposition. Eigenvalues for the first and second DCA axis on the abundance matrix were 0.238 and 0.126. Axis 1
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R. Menéndez, D. Gutiérrez
Figure 1. Successional variation in the number of individuals of five beetle taxa inhabiting dung pats (— May and ---- July). M, Sample size in May; J, sample size in July.
was interpreted as pat age since samples were ordinated along the first axis in increasing pat age (r2 = 0.61, F = 20.32, df = 1, 13, P < 0.001, figure 2). Moreover, pats of a given age in July tended to show lower axis 1 scores than those in May. Axis 2 was not associated either with pat age or with months. According to the interpretation of axis 1, there was a taxonomic replacement throughout the successional process. Sphaeridium and Cercyon were associated with fresh pats, Scarabaeidae with mid-age pats and Aphodiidae and Staphylinidae with old pats. Successional mean occurrence values (SMO) were higher in May than in July for all beetle groups (table I). SMO in May was positively correlated with SMO in July (r = 0.96, n = 5, P = 0.003). Sphaeridium showed the lowest SMO values because average abundance occurred on the first days of the succession; in contrast, the late occurrence of Aphodiidae and Staphylinidae is shown by their higher SMO values.
Figure 2. Ordination of sampling pats varying in age (d, May; s, July) (a), and beetle taxa (b) by detrended correspondence analysis. The ordination space is identical in both figures. The number next to each symbol is the age of the pat in days (a). (b) Names of the beetle taxa (Sphae, Sphaeridium; Cercy, Cercyon; Scara, Scarabaeidae; Aphod, Aphodiidae; Staph, Staphylinidae).
3.2. Successional patterns of coprophagous species A total of 581 dung beetles belonging to twelve Aphodius species were caught. Except A. obscurus, all species arrived on the pats during the first 3 d (table II). Eigenvalues for the first and second DCA axis Acta Oecologica
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Table I. Successional mean occurrence (SMO) in days for five beetle groups recorded in two sampling months. Values are given as mean ± 1 SD, with sample sizes in brackets. Statistical significance of ANOVA (F) and Mann-Whitney (U) tests are shown in the last column. * Log-transformed data. Taxa Hydrophilidae: Sphaeridium Cercyon Scarabaeidae Aphodiidae Staphylinidae
May
July
2.7 ± 0.4 (5) 4.1 ± 0.3 (5) 4.1 ± 1.4 (5) 10.0 ± 1.6 (5) 8.7 ± 1.6 (5)
1.8 ± 0.1 (5) 2.5 ± 0.3 (5) 3.0 ± 0.1 (5) 4.3 ± 0.3 (5) 4.5 ± 0.5 (5)
F* = 4.64, P = 0.06 F = 13.90, P = 0.006 U = 16, P > 0.2 F* = 20.38, P = 0.002 F* = 7.30, P = 0.03
Table II. First date of occurrence and successional mean occurrence (SMO) in days for all Aphodius species recorded in two sampling months. Species
A. prodromus A. erraticus A. fimetarius A. conspurcatus A. pusillus A. depressus A. haemorrhoidalis A. fossor A. obscurus A. ater A. scybalarius A. rufipes
May SMO
n
1 3 2 3 1 1 1 1 10 1
2.11 3.00 3.00 3.00 4.09 8.44 8.90 11.97 12.43 13.67
2 2 2 1 184 10 15 3 2 133
were, respectively, 0.372 and 0.197. Neither axis 1 nor axis 2 was correlated with dung pat age (P > 0.5). SMO values in May were not correlated with SMO values in July (r = –0.17, n = 7, P = 0.716). On other hand, the successional widths (SD) of Aphodius species were positively correlated to successional mean occurrence (SMO) both in May (r = 0.80, n = 9, P = 0.009) and in July (r = 0.93, n = 8, P = 0.001). SMO values of Aphodius species ranged from 2.11 to 13.67 in May and from 1 to 7.95 in July (table II). However, this did not imply a significantly more even distribution than expected at random (table III). The probability that a randomly generated community showed parameters more evenly distributed than the actual assemblage was higher than 0.05 in most cases. VAR value in May was the only statistically significant comparison. Likewise, mean successional overlap (PS) was 0.299 in May and 0.392 in July. These values were not Vol. 20 (5) 1999
July
First date
First date
SMO
n
1 2
1.00 7.95
2 10
1 1 2 2
3.86 2.00 5.64 3.11
53 25 51 9
1 2 2
3.49 2.50 3.00
72 2 3
significantly lower than those randomly expected (P = 0.851 in May and P = 0.916 in July). 4. DISCUSSION The results presented here show that there was a faunal turnover of beetles inhabiting dung pats in Table III. One-tailed P-level probabilities for minimum (MIN) and variance (VAR) of SMO differences between Aphodius species for the whole assemblages in May (30-d axis) and July (10-d axis). Probabilities are the ratio between the number of random iterations showing higher MIN values, and lower VAR values than observed values, and the total number of iterations (3 000 random assemblages for each sampling month). Parameters
MIN VAR
Observed values
Probabilities
May
July
May
July
0.000 2.180
0.110 0.609
1.000 0.036*
0.391 0.423
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relation to age of dung. A taxonomic sequence was observed throughout the process of dung decomposition: Hydrophilidae (Sphaeridium and Cercyon), Scarabaeidae, Aphodiidae and Staphylinidae. The same taxonomic sequence was observed on two occasions during the season, though succession proceeded somewhat faster in July than in May. This fact may be attributable to different weather conditions over the season [19, 36, 37]. Temperature increases the bacterial activity and the loss in moisture content in dung pats, leading to an accelerated successional process [22, 35, 38]. Similar successional patterns have been found for dung beetle assemblages in other temperate regions [11, 32, 34, 36]. Differences in successional occurrence between groups have been attributed to differences in food requirements and resource availability [8, 34]. Dung pats are maximally distinct from their surroundings at the moment of their origin and guilds of specialist species are the first colonisers, while soil generalist and predator species progressively colonise the dung pats as they become more similar to their surroundings [21]. Carnivorous beetles seem to be largely dependent on the number of suitable preys in droppings. The main food of Staphylinidae species consists of larvae of flies and dung beetles, which are not available during the first days of succession [34]. Dung beetle larvae in dung pats consume dung in a seemingly unselective manner [29] while adults typically use dung juices [22, 23, 35]. A dung pat represents a highly concentrated parcel of energy, but it contains resources which disappear under the effects of microbial activity and physical factors [31]. Competition could be severe in ephemeral habitats because the nutrient availability is maximum at the beginning, subsequently decreasing with time. A strategy of arriving in the dropping as early as possible could be advantageous for specialist coprophagous that are able to ensure a portion of the resource for exclusive use, but not for species that stay and potentially compete for a prolonged period of time [22, 25]. This hypothesis could explain the differences between SMO of Scarabaeidae and Aphodiidae, since these taxa show contrasting breeding behaviours. In most cases, Scarabaeidae species do not feed within dung pats, but are nesting beetles which dig a vertical tunnel under or outside the pat and then transport dung to the bottom of the burrow [17]. Thus, a portion of the resource is protected against competitors and climatic conditions, and may be used for both larval and adult feeding [4]. An early arrival in dung
R. Menéndez, D. Gutiérrez
pats could provide a crucial advantage for nesters because they are able to remove rapidly a portion of resource for their exclusive use [22]. Nevertheless, only one species (Onthophagus similis) accounted for 98 % of Scarabaeidae caught, hence the successional patterns observed for Scarabaeidae as a whole might be largely determined by the requirements of that species. In contrast, the larval development and adult feeding of most Aphodius species take place within dung pats [4], and therefore, they are not able to monopolise a portion of dung. In this case, a successional segregation in resource use could be expected. However, results from the null models gave no evidence of such successional segregation of Aphodius species, not supporting competition as a possible explanation for the differences in successional occurrence of species [30]. Our results on competition in Aphodius species were based on the outcome of null models. Even random models are based upon a number of assumptions which will determine their predictions. Though some assumptions are implicit in all tests of niche differentiation and can only be regarded as an inevitable approximation (see [48] for a discussion), others have considerable effects on the outcome of the tests and must be discussed in order to understand the limitations when applying the model [39]. First, a critical decision is how to define the important interacting species to be considered in the analysis. To test competitive displacement obviously only species that constitute a guild, as those sharing a resource, should be included [7, 48]. Thus, Aphodius species were treated as a single guild at least when considering potential interactions among adults, given the similarity of adult feeding methods [4]. However, dominant species could show greater niche complementariness than the whole community [39], and significant niche differences between dominant species could not be detected if all coprophagous species are considered. We performed additional analyses including only the four most abundant species in each month, but they produced similar results to those for the whole assemblage (table IV). The values of mean successional overlap for this subset were not significantly lower than those randomly expected either (P > 0.05). Second, a uniform distribution of resource must be assumed when testing competitive displacement in resource use within communities [26]. Nutritional requirements of Aphodius species are insufficiently known; although adult beetles obtain all or most of their nutrition from dung juices, the specific comActa Oecologica
533
Heterotrophic succession in dung beetles
Table IV. One-tailed P-level probabilities for minimum (MIN) and variance (VAR) of SMO differences between Aphodius species for subsets of the whole assemblages in May and July. Probabilities as in table III. Parameters
All species, 10-d axis MIN VAR Four abundant species, 30-d axis MIN VAR Four abundant species, 10-d axis MIN VAR
Observed values
Probabilities
May
July
May
July
0.000 0.615
– –
1.000 0.383
– –
0.460 5.647
– –
0.863 0.138
– –
0.694 0.657
0.370 1.005
0.375 0.273
1.000 0.091
pounds used have not been studied [2, 22]. Adult resource availability seems to be dependent on the water content in the dung, and dung containing moisture values lower than 68 % could be unsuitable for some coprophagous species [10]. The water content in a dung pat decreases relatively slowly during the first 10 d and moisture values are frequently higher than 75 % during this time period [16, 31]. Given the difficulty of clearly defining the availability of resources in the pat, we performed additional null model tests using an endpoint of 10 d in May, which assumes that the chemical composition of resources was relatively constant during that period. These analyses, however, produced no significant results either for successional mean occurrence (table IV) or for mean successional overlap (P > 0.05). Our results of the null model tests were not significant for most cases, and both the set of species selected and the time scale considered had no effect on the outcome of the tests. Although non-significant results do not mean that the alternative hypothesis must be rejected, it seems unlikely that interspecific differences in adult successional occurrence have been the result of past or present competition interactions. Competition might not be a major factor if the resource is not limited. Holter [30] showed that the Aphodius guild inhabiting a dung pat requires only a negligible fraction (0.3 %) of the initial energy in the dung. On the other hand, interspecific differences in SMO were not consistent between sampling months and there was no clear species turnover over the successional process. This was not in agreement with Gittings and Giller [16] who found a successional species turnover of Aphodius species over dung pat decomposition. In our study, dung pat age did not Vol. 20 (5) 1999
determine species composition because most of the species were present in the dung pat during the first 10 d, and only a few was present in old pats. Differences in SMO between species could be simply the result of differences in residence time within dung pats [20]; this explanation was supported by the positive relationship between successional mean occurrence and standard deviation. Most species arrive early on the pats (first and second days, see table II), but some species stay longer in a given dropping than others. It is difficult to identify the main reason for these differences. Fresh dung pats could attract more beetles than old pats because coprophagous beetles use their olfactory senses to locate dung pats [35, 40]. Thus, adults mainly colonise fresh dung pats and leave them when the drying of dung makes it unsuitable as food [33]. However, adult activity in the pats could reflect other requirements, such as mating, egg-laying, or larval feeding [20]. For instance, immature females of A. ater tended to occur in fresher pats than mature females, because females colonised fresh pats and matured reproductively within them [27]. Moreover, Aphodius species differ in oviposition behaviour and these differences may be important in determining species succession [15, 16]. Early successional species lay their eggs in the soil because wet dung is not suitable for eggs and larval survival, while mid and late species lay their eggs in dung. Though oviposition behaviour was not known for all species included in the present study, our results seem to be relatively consistent with that hypothesis. Thus, soilovipositing species (e.g. A. prodromus, A. erraticus, A. rufipes) showed smaller SMO than dung-ovipositing species (A. fimetarius, A. fossor, A. ater).
534
The present results suggest that the facilitation model of succession [6] is supported by the successional process in dung pats, as many late-arriving species seem to benefit from the activity and population growth of the early arrivals. The food availability and microclimatic conditions around dung seem to determine the successional occurrence of beetle taxa. In dung beetle succession, interspecific competition is not likely to occur among adults because beetle density is low relative to resource supply. The drying of dung may be the decisive factor in determining pat colonisation by coprophagous species, while the residence time in the pat could reflect other specific requirements (mating, egg-laying and larva feeding requirements). Acknowledgments We thank Marcos Méndez for assistance with the field work and Silvino Menéndez for carrying out the Turbo Pascal subroutines. Robert J. Wilson kindly improved the English. José R. Obeso and two anonymous referees provided useful criticism on an earlier version of the manuscript. A. M. Felicísimo kindly provided climatic data. The Instituto para la Conservación de la Naturaleza (ICONA) provided funds, climatic data and permission for trapping beetles in the Picos de Europa National Park.
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