Diel separation of Afrotropical dung beetle guilds - avoiding competition and neglecting resources

Diel separation of Afrotropical dung beetle guilds—avoidingcompetition and neglecting resources (Coleoptera: Scarabaeoidea)

SYLVIA KRELL-WESTERWALBESLOH{{, FRANK-THORSTEN

KRELL{* and K. EDUARD LINSENMAIR{

{Lehrstuhl fur Tierokologie und Tropenbiologie, Biozentrum, Universitat

Wurzburg, Am Hubland, D-97074 Wurzburg, Germany

{Soil Biodiversity Programme, Department of Entomology, The Natural

History Museum, Cromwell Road, London SW7 5BD, UK

(Accepted 15 July 2003)

Dung beetle guilds of different competitive level coexist at high abundances inthe forest–savanna mosaic of Ivory Coast. A total of 25 875 specimens wasrecorded from 90 samples of fresh buffalo dung exposed for 4-h periods over theday in the Parc National de la Comoe. Redundancy analyses show differentpatterns of the guild structure determined by time of day, and positivecorrelations of guild abundance with temperature. The competitively superiortelecoprids (rollers) have their abundance peak at midday when the hightemperatures presumably enable them to perform their energetically costlyrolling behaviour at greater speed. The competitively intermediate paracoprids(tunnellers) and the competitively inferior endocoprids (dwellers) have their peakaround dusk when: (1) the superior competitors are not active, and (2) they caneasily synchronize their flight activity using light intensity changes. During thetwo peaks of flight activity of the dung beetles, their abundance at the resource isvery high, causing obvious competition. On the other hand, the resource ishardly used between 22:00 h and 10:00 h. This is probably due to physiologicalconstraints (high optimum temperature required for the diurnal species anddependence on light intensity patterns as a flight trigger of the nocturnal species,respectively). Shifting flight activity to these periods of low competition does notoccur, resulting in a unequal level of competition over the day, thus periods ofconsiderable competition within dung beetle assemblages alternate with vacanttemporal refuges.

KEYWORDS: Coleoptera, Comoe National Park, Cote d’Ivoire, diel separation,dung beetles, Guinea savanna, temporal resource partitioning, Scarabaeidae.

Journal of Natural HistoryISSN 0022-2933 print/ISSN 1464-5262 online # 2004 Taylor & Francis Ltd

http://www.tandf.co.uk/journalsDOI: 10.1080/00222930310001618921

*Author to whom correspondence is addressed; e-mail: [email protected]

JOURNAL OF NATURAL HISTORY, 2004, 38, 2225–2249

Introduction

‘‘Quel est celui-ci qui trottine vers le monceau, craignant d’arriver trop tard?’’

(Jean-Henri Fabre, Le Scarabee Sacre, 1879)

If a resource is an unpredictable, ephemeral patch, it is crucial for the success of

any potential user to be in the right place at the right time. This is the more so if

the ephemeral nature of the resource is caused by the users themselves, as in rapid

degradative successions (Begon et al., 1996: 693). Interspecific competition is

inevitable on ephemeral resource patches that are used by different species in high

abundance. Dung pats in humid Afrotropical savannas during the rainy season

are a good model system with which to study strategies of exploiting ephemeral

resource patches. The exact time and place of the appearance of faeces is

unpredictable, in natural habitats they are patchily distributed. Furthermore, they

are used up by dung beetles mostly within less than 24 h. The succession of dung

beetle assemblages in temperate regions (at least in large droppings) generally

follows the facilitation model of Connell and Slayter (1977) (Beaver, 1984; Hanski,

1991): resource exploitation by later users is facilitated by the action of the

first users. In contrast, in humid African savannas the early occupants of a dung

pat tend to use the resource more or less completely (figures 1, 2). Hence, the

succession seems to follow the inhibition model (Connell and Slayter, 1977): the

action of first users inhibits exploitation by later arrivals, because after the first

users have exploited the substrate, only a small fraction is left, which is relatively

unproductive for any later arriving beetles. Possible successful strategies in such a

FIG. 1. Typical buffalo dung pat exposed during the day well before dusk. Users are mostlytelecoprids.

2226 S. Krell-Westerwalbesloh et al.

system are either to be competitively superior (effectively monopolizing parts of the

resource) or to avoid competition (using the resource when superior competitors are

not active).

Dung beetles

Coprophagous scarab beetles (Scarabaeidae) use their resource in different

ways, through which they can be classified into guilds (Bornemissza, 1969;

Cambefort and Hanski, 1991). The guilds show a dominance hierarchy in the

competitive ability of their species (Doube, 1990). Species of the roller guild

(telecoprids) rapidly form balls from the faeces, roll them away from the food

source, and deposit them in or on the soil to ensure the exclusive use of this part

of the resource. Formation of a ball generally takes much less than 1 h, and in the

small Sisyphini only a few minutes (Halffter and Matthews, 1966: 103; Doube,

1990; personal observation). The tunnellers (paracoprids) make nests directly under

the food source and transport dung into the nest where they form dung balls. This

is relatively time-consuming and takes at least a few hours (Doube, 1990). Dwellers

(endocoprids) feed and reproduce directly in the dung pat. Kleptoparasites use

faeces portions monopolized by species of telecoprids or paracoprids. They

penetrate dung balls made by telecoprids, or the dung mass in the subterranean

nests of paracoprids.

If the beetles of all guilds are abundant, these modes of resource utilization are

mutually exclusive: when the dung is rolled away by rapid telecoprids (figure 1),

FIG. 2. Typical buffalo dung pat exposed just before dusk or early at night. Users aremostly paracoprids. The big soil mounds were produced by Coprini (large paracoprids).

Diel separation of dung beetle guilds 2227

paracoprids do not have enough left to bury. When the dung is rolled away or

buried (figure 2), the endocoprids have nothing to lay their eggs in. The com-

petitively superior species are, therefore, the fast telecoprids, the least competitive

species are the endocoprids (Doube, 1990). The success of kleptoparasites depends

on the success of their hosts. Dung relocation (rolling and tunnelling) is burdened

with high energetic costs whereas endocoprid behaviour and kleptoparasitism is

much less energetically costly.

Because dung usually persists for less than 24 h as a usable resource in

the humid African savannas during the rainy season, success of any species is

determined mostly by its early arrival at the resource (Doube, 1987; Hanski, 1989:

‘extreme priority effect’), especially because telecoprid and paracoprid species are

able to monopolize a part of the resource. Therefore, the diel activity of the species

is an important parameter determining their success (Hanski, 1990). The rapidity of

colonization of a freshly emerged resource is enormous. Anderson and Coe (1974)

found that 16 000 beetles had completely removed a 1.5 kg pile of elephant faeces

within 2 h in the Tsavo National Park, Kenya. A normal portion of human faeces

is generally removed completely after 3 h in our study area (Parc National de la

Comoe, Cote d’Ivoire) if it has been deposited during the day in the savanna

parkland (personal observation). Despite this strong competition between rapid,

abundant users, species of different competitive potency occur syntopically in

African savanna parklands.

Did competitively inferior guilds evolve mechanisms for avoiding competition

or do they depend on random success to coexist with superior competitors?

Temporal resource partitioning

Although temporal resource partitioning is considered to be less common

compared to spatial separation and trophic specialization (Schoener, 1986), it is

a widespread mechanism to avoid competition between closely related species or

phylogenetically distant groups. The most common type of temporal separation is a

different phenology, especially seasonally different activity times in using a resource

(Wolda, 1988). Diel resource partitioning within animal assemblages, however, has

rarely been analysed (Remmert, 1976; Southwood, 1978; Loser, 1980; Dennison

and Hodkinson, 1983; Jaksic, 1983). Diel resource partitioning within dung beetle

assemblages has been studied a few times at species level (e.g. Caveney et al., 1995:

paracoprid Onitis spp.; Hanski, 1986: endocoprid Aphodius spp.; Walter, 1985:

not quantitatively) or at genus level (e.g. Peck and Forsyth, 1982: dung beetle

assemblages in Ecuador). Diel separation between guilds has only once been

quantitatively examined (Doube, 1991), but in those assemblages, endocoprids were

extremely rare.

In a parallel study (Krell et al., 2003), we found that guild structures of beetle

assemblages in buffalo dung differ between day and night. We also found that the

abundance (and biomass, unpublished results) of dung beetles is at an obviously

non-competitive level all day and night in the gallery forest and during the day in

the grassland of the river valley. In the savanna parkland, however, the number of

dung beetles seems to be very high at night and during the day. Does competition

always control the structure of coprocenoses (animal assemblages in dung) in the

savanna habitat or are our former results artefacts of low temporal resolution?

In the present study we increased resolution by studying the dung beetle


assemblages that have populated dung portions during defined 4-h periods to

determine the diel patterns of flight activity and resource partitioning of the

different dung beetle guilds.

Having analysed pooled data from different habitats, Krell et al. (2003) found

that the abundance of telecoprids and their kleptoparasites is positively correlated

with the temperature of faeces and soil, whereas the number of endocoprids

increases with decreasing temperature during the exposure period. Thus, the

competitively most inferior group seems to be tolerant to unfavourable climatic

conditions. The higher temporal resolution of the present study will show whether

these climatic parameters influence the abundance of guilds in the savanna or

whether they are irrelevant in influencing guild structure within one habitat.

Study area

We conducted our experiments in the southern part of the Parc National de la

Comoe in north-eastern Ivory Coast (~Cote d’Ivoire, West Africa) around the

research camp of the University of Wurzburg (Lola-Camp; see Krell et al., 2003:

figure 1). The study area is at the border between the Guinea and Subsudan

savanna attributed by Porembski (1991) to the former and by Poilecot (1991),

amongst others, to the latter. Savanna parkland takes up the largest area, followed

by forest islands, gallery forest and minor habitat types. Since in the savanna

parkland the abundance of dung beetles is high both at night and during the day

(Krell et al., 2003), we studied diel activity patterns on a site in this habitat. It is the

same savanna site used for the study of habitat patterns by Krell et al. (2003:

figure 4; 3‡48’58@W, 8‡45’02@N).

Methods

Experiments

From 7 May to 12 July 1997 (beginning of the rainy season to the beginning

of the ‘Little Dry Season’ in the middle of the rainy season; Ojo, 1977: 97) we

deposited portions of 1 kg (900 ml) of faeces of buffalo (Syncerus caffer (Sparrman))

on the soil during 4-h periods starting 2:00 h, 6:00 h, 10:00 h, 14:00 h, 18:00 h

and 22:00 h (15 samples each; see Appendix). The exposure periods were spread

randomly over the study period with two to four dung portions exposed

simultaneously. After the exposure period, the faeces, and soil beneath that had

been populated by coprophagous beetles, were floated in a bucket of water. In

addition, we searched the complete sediment in the bucket for remaining beetles. A

detailed description and discussion of the method is given by Krell et al. (2003).

We did not use traps because we wanted to record established coprocenoses after a

fixed period of exposure of the resource, not all of the beetles visiting the resource

during a period of time. Some beetles may approach the dung pat but fly away after

a short exploration (personal observations) or when the pat is already highly

populated (Landin, 1961: 207). With our method we register only the actual users

of a resource whereas traps collect both users and tourists. Traps overestimate

the portion of some groups containing many tourists. These groups cannot be

unambiguously identified among the trapped beetles. However, with our method we

underestimate the proportion of telecoprids in the coprocenoses since many of them

have already left the pat before we collected the sample. Although we obviously got


a biased pattern, we are able to identify the bias, whereas in pitfall trap sampling

the overestimated groups are not recognizable.

The abundance of scarab beetles increases strongly after heavy rainfall (Walter,

1985; personal observation). During a period of heavy rain (11–23 June) we did not

expose any dung (see Appendix).

The collected material (25 875 specimens) will be incorporated into the

collection of The Natural History Museum, London. The specimens were identified

by F.-T.K.

Microclimatic change during the day

To find possible correlations of guild abundances with microclimatic parameters

we measured:

(1) air temperature at about 1 m above ground at the beginning and end of the

exposure period;(2) soil temperature at a depth of 1 and 10 cm at the beginning and end of the

exposure period;(3) dung temperature just before collecting the sample (1–3: microcomputer

thermocouple thermometer HI 9063, Hanna Instruments);(4) relative air humidity (RH) at about 1 m above the ground at start and end

of the exposure period (electronic hygrometer HI 9064, Hanna Instruments).

Since the instrument is reliable up to 95% RH, all measurements above 95%

are counted as 95%. This reduces the arithmetic means of RH during the

night periods (table 3), which is certainly closer to 100%.

Guild classification

We treat each species as belonging to exactly one guild. The term ‘guild’ is used

as in its original definition as a group of species which use the same resource in

a similar way regardless of their phylogenetic relationships (cf. Simberloff and

Dayan, 1991). However, we confine this analysis to the dung beetles of the family

Scarabaeidae which are by far the major users of the dung resource. Other

coprophilous beetles (Histeridae, Hydrophilidae, Carabidae, Staphylinidae) are

either predators, occur in relatively low numbers in the studied assemblages or use

the resource in different ways. We follow the rough classification of coprophagous

members of the coprocenoses into the guilds of telecoprids (rollers), paracoprids

(tunnellers), endocoprids (dwellers) and kleptoparasites (Bornemissza, 1969;

Cambefort and Hanski, 1991) but we divide the last group into kleptoparasites

of paracoprids and those of telecoprids (Cambefort, 1991). As usual, there is no

simple correlation between higher taxa and guilds. In the studied assemblages, the

guilds consist of the following members (for sources and more detailed discussion

of the guild classification see Krell et al., 2003):

. telecoprids (rollers): all Gymnopleurini, all Sisyphini, all Canthonini (only

Anachalcos spp.) (Scarabaeini were not present and are generally very rare in

the study area; personal observation);. paracoprids (tunnellers): all Coprini (including Dichotomiini), all Onitini,

most Oniticellini, most Onthophagini, Aphodius (Neocolobopterus) maculi-

collis Reiche;. endocoprids (dwellers): all Aphodiinae (except Aphodius maculicollis),

Oniticellus formosus Chevrolat;


. obligatory kleptoparasites:(a) of paracoprids: Pedaria spp., Onthophagus juvencus Klug;

(b) of telecoprids: Cleptocaccobius spp., Hyalonthophagus nigroviolaceus

(d’Orbigny), Onthophagus lioides d’Orbigny, O. tersipennis d’Orbigny.

Statistics

For the statistical analyses we used the computer programs Canoco for

Windows 4.0 (Centre for Biometry, Wageningen, The Netherlands), SsS 1.1a

(Rubisoft Software GmbH, Eichenau, Germany) and XLSTAT 4.4 (Thierry

Fahmy, Paris, France).

Correlations between the abundance of guilds are shown by a standardized

principal component analysis (PCA) (Canoco) using log-transformed guild

abundance data. PCA requires a normal distribution for each guild which is not

present in all our data, even when log-transformed (telecoprids and both groups

of kleptoparasites; Kolmogoroff-Smirnoff test, SsS), but for merely descriptive

purposes, larger departures from ideal data structure are tolerable (Greig-Smith,

1980; Gauch, 1982: 137). Significance of the correlations was tested with the non-

parametric Spearman Rank Correlation Coefficient (XLSTAT) using the critical

values given by Zar (1996).

A standardized redundancy analysis (RDA) (Canoco; Jongman et al., 1995;

Legendre and Legendre, 1998) using log-transformed guild abundance data shows

the relationship between environmental parameters and guild abundances. The

highest increase of temperature during the exposure period was re-scaled to 0; the

highest decrease becomes the highest value.

Results

Diel differences in abundance and guild structure of coprocenoses

Both the ratios of dung beetle guilds and the overall abundance of dung beetles

was extremely unequally distributed over the day. The two peaks of overall

abundance were at midday (48%; 829 individuals per kg dung) and around dusk

(25%; 429 ind. per kg dung) (figure 3; table 1). Since we underestimate the number

of telecoprids (Krell et al., 2003), the real peak at midday is higher than shown in

figure 3 and, hence, much higher than the peak at dusk. It is even possible that there

is no local minimum at 14:00–18:00 h. The dung beetles have their lowest flight

activity during the night until dawn. Less than 4.5% of all dung beetles in our

samples flew between 22:00 h and 6:00 h (38 ind. per kg dung). The guild structure

of dung beetle assemblages over the day is given in table 1.

Diel separation and correlation of guilds

The PCA (figure 4) shows graphically the distribution of samples in a two-

dimensional space considering the highest possible proportion of overall variability.

Day and night samples are clearly separated with only a slight overlap by samples

from the period just after dawn. All samples from the periods of highest flight

activity [around dusk (18:00–22:00 h) and midday (10:00–14:00 h)] are isolated with

only a slight overlap of the latter with other daytime periods. The 6:00–10:00 h and

14:00–18:00 h samples and the 22:00–2:00 h and 2:00–6:00 h samples are mixed,

respectively.


All dung beetle guilds but the paracoprids have one diel abundance peak

(table 2); 79% of the telecoprids fly around noon; 80% of their kleptoparasites are

active between 10:00 h and 18:00 h; 84% of the endocoprids fly around dusk.

Paracoprids search for food during the hot hours of the day (39%) and around dusk

(46%) whereas their kleptoparasites have only one abundance peak (83%) around

dusk.

Flight activity times of telecoprids and their kleptoparasites are positively

correlated as graphically shown by a PCA in figure 4 (Spearman rank correlation

coefficient 0.65; Pv0.001). The flight activity of kleptoparasites of paracoprids

and their hosts is, however, only slightly positively correlated but still statistically

significant (0.23; Pv0.02). The angle between the axes of the endocoprids

(supposed competitively inferior) and of the telecoprids (supposed competitively

superior) is much more than 90‡ indicating a negative correlation (20.52;

Pv0.001). The negative correlation between paracoprids (supposed competitively

intermediate) and endocoprids is not statistically significant, but the positive

correlation between telecoprids and paracoprids is significant (0.41; Pv0.001).

Guild structure and environmental variables

The microclimatic parameters of the three habitats are given in table 3. Air and

soil temperatures increase between 6:00 h and 14:00 h and decrease during other

times of the day. In our measuring regime, faeces have the highest temperature at

14:00 h and the lowest at 6:00 h with an average difference of 14‡C. Relative air

humidity reaches more than 90% after dusk and decreases only in the morning.

FIG. 3. Diel flight activity of dung beetle guilds, indicated by cumulative abundance in 15samples per 4-h period. Klepto/Tele, kleptoparasites of telecoprids; Klepto/Para,kleptoparasites of paracoprids.


Table 1. Guild structure of dung beetle assemblages in savanna parkland during different times of day (4-h periods), pooled numbers of 15 sampleseach (the last row shows the number of dung beetles per period and its proportion of the overall number of dung beetles that we obtained in ourexperiment).

Period 2:00–6:00 h 6:00–10:00 h 10:00–14:00 h 14:00–18:00 h 18:00–22:00 h 22:00–2:00 h Total

Guild N % N % N % N % N % N % N %

Endocoprids 51 6.46 31 1.45 4 0.03 78 2.09 1 795 27.91 172 48.45 2 131 8.24Paracoprids 654 82.78 579 27.02 2 514 20.23 1 176 31.55 4 362 67.82 114 32.11 9 399 36.32Telecoprids 34 4.30 997 46.52 8 559 68.87 1 243 33.35 22 0.34 45 12.68 10 900 42.13Klepto.Para. 12 1.52 23 1.07 3 0.02 0 0.00 197 3.06 2 0.56 237 0.92Klepto.Tele. 39 4.94 513 23.94 1 348 10.85 1 230 33.00 56 0.87 22 6.20 3 208 12.40Total 790 3.05 2143 8.28 12 428 48.03 3 727 14.40 6 432 24.86 355 1.37 25 875

N, Number of individuals; Klepto.Para., kleptoparasites of paracoprids; Klepto.Tele., kleptoparasites of telecoprids.

Diel

sepa

ratio

no

fd

un

gb

eetleg

uild

s2

23

3

Relationships between environmental parameters and guild abundances over

the day are shown by an RDA (figure 5). Endocoprids and kleptoparasites of

paracoprids are clearly associated with the period around dusk and obviously not

negatively affected by cooling of air and soil during that period. Telecoprids and

their kleptoparasites prefer the hottest time of the day (10:00–14:00 h) and are

closely related to the temperature of faeces, soil and air at the end of the exposure

period. The paracoprids are more related to soil and air temperature at the

beginning of the exposure period. The relative humidity is negatively correlated

with the abundance of paracoprids and kleptoparasites of telecoprids and rather

uncorrelated with the other guilds.

FIG. 4. Biplot of PCA of log-transformed absolute numbers of individuals within each guild[mapping of the data (samples) simultaneously with the mapping of the initial of thevariables (guilds) on the factorial axes]. Eigenvalues: component 1, 0.639; component2, 0.200. Endo, endocoprids (dwellers); Klepto.P, kleptoparasites of paracoprids;Klepto.T, kleptoparasites of telecoprids; Para, paracoprids; Tele, telecoprids (rollers).(#) 6:00–10:00 h samples; (%) 10:00–14:00 h samples; (e) 14:00–18:00 h samples; (.)18:00–22:00 h samples; (&) 22:00–2:00 h samples; (¤) 2:00–6:00 h samples.


Table 2. Proportion (%) of dung beetle guilds in savanna parkland by time of day(individually rounded); for number of individuals see table 1.

Period Endocoprids Paracoprids Telecoprids Klepto.Para. Klepto.Tele.

2:00–6:00 h 2.39 6.96 0.31 5.06 1.226:00–10:00 h 1.45 6.16 9.15 9.70 15.99

10:00–14:00 h 0.19 26.75 78.52 1.27 42.0214:00–18:00 h 3.66 12.51 11.40 0.00 38.3818:00–22:00 h 84.23 46.41 0.20 83.12 1.7522:00–2:00 h 8.07 1.21 0.41 0.84 0.69

Klepto.Para., kleptoparasites of paracoprids; Klepto.Tele., kleptoparasites of telecoprids.

Table 3. Abiotic parameters of microhabitats (arithmetic means of measurements¡SD).

Parameter2:00–6:00 h

6:00–10:00 h

10:00–14:00 h

14:00–18:00 h

18:00–22:00 h

22:00–2:00 h

T air start 24.6¡0.6 23.0¡1.0 29.2¡1.3 32.1¡2.4 30.4¡4.2 25.5¡2.2(N~5) (N~5) (N~4) (N~5) (N~6) (N~5)

T air end 24.3¡1.5 28.0¡1.9 34.1¡1.6 29.6¡2.7 26.2¡2.3 24.6¡1.8(N~5) (N~5) (N~4) (N~5) (N~6) (N~5)

DT air 20.4¡1.4 z4.9¡1.2 z5.0¡1.8 22.5¡1.5 24.2¡2.1 20.9¡0.8(N~5) (N~5) (N~4) (N~5) (N~6) (N~5)

T soil 1 cm start 27.1¡1.7 24.8¡1.0 35.1¡2.5 37.6¡3.2 32.9¡3.9 29.3¡3.3(N~15) (N~15) (N~15) (N~15) (N~15) (N~15)

T soil 1 cm end 26.2¡1.5 31.1¡2.0 41.8¡3.8 31.5¡1.9 28.7¡2.3 27.1¡2.1(N~15) (N~15) (N~15) (N~15) (N~15) (N~15)

DT soil 1 cm 20.9¡1.0 z6.3¡1.8 z6.6¡3.7 26.1¡1.6 24.2¡1.8 22.2¡1.4(N~15) (N~9) (N~15) (N~15) (N~15) (N~15)

T soil 10 cm start 28.5¡1.9 26.4¡1.2 30.7¡1.3 34.4¡1.4 34.3¡4.1 32.2¡3.9(N~15) (N~15) (N~10) (N~15) (N~15) (N~15)

T soil 10 cm end 27.6¡2.0 28.9¡1.9 37.5¡2.0 32.7¡1.6 31.1¡3.2 29.7¡2.9(N~15) (N~15) (N~15) (N~15) (N~15) (N~15)

DT soil 10 cm 20.9¡1.1 z2.6¡1.5 z6.7¡1,8 21.7¡1.0 23.2¡1.9 22.5¡1.3(N~15) (N~15) (N~15) (N~15) (N~15) (N~15)

RH air start (%) 95¡0.0 95¡0.0 79.6¡5.8 72.2¡9.1 72.7¡15.1 89.8¡6.4(N~5) (N~5) (N~4) (N~5) (N~6) (N~5)

RH air end (%) 94.2¡0.8 92.2¡2.8 62.8¡10.4 73.8¡12.4 90.0¡7.9 94.6¡0.9(N~5) (N~5) (N~4) (N~5) (N~6) (N~5)

T faeces end 25.6¡1.2 29.3¡2.0 39.6¡1.9 32.5¡1.7 29.3¡2.4 27.1¡2.1(N~15) (N~15) (N~15) (N~15) (N~15) (N~15)

N, Number of measurements; T air start, air temperature at start of the experiment; T airend, air temperature at the end of the experiment; DT air, difference between airtemperatures at start and at the end of the experiment; T soil 1 cm start, soil temperature(1 cm depth) at start of the experiment; T soil 1 cm end, soil temperature (1 cm depth) at theend of the experiment; DT soil 1 cm, difference between soil temperatures (1 cm depth) atstart and at the end of the experiment; T soil 10 cm start, soil temperature (10 cm depth) atstart of the experiment; T soil 10 cm end, soil temperature (10 cm depth) at the end of theexperiment; DT soil 10 cm, difference between soil temperatures (10 cm depth) at start and atthe end of the experiment; RH air start, relative air humidity at start of the experiment; RHair end, relative air humidity at the end of the experiment; T faeces end, dung temperature atthe end of the experiment.


Nine of the parameters (environmental variables and times of the day) are

potentially relevant for the interpretation of diel guild patterns since their

eigenvalues in the RDA are higher than 0.2 (table 4). The most important

parameters that possibly affect guild structure are the temperatures of air and soil

(1 cm) at the end of the exposure period, closely followed by the faecal temperature.

FIG. 5. RDA ordination biplot of guilds and environmental variables based on log-transformed guild abundance data of all samples. Eigenvalues: axis 1, 0.577; axis 2,0.162. (,) Centroids of times of the day (categorical variables); Endo, endocoprids(dwellers); Klepto.P, kleptoparasites of paracoprids; Klepto.T, kleptoparasites oftelecoprids; Tele, telecoprids (rollers); diffTair, difference between air temperatures atstart and at the end of the experiment; diffTsoil, difference between soil temperatures(1 cm depth) at start and at the end of the experiment; RHend, relative air humidity atthe end of the experiment; RHstart, relative air humidity at start of the experiment;Tair end, air temperature at the end of the experiment; Tair start, air temperature atstart of the experiment; Tfaeces, dung temperature at the end of the experiment;Tsoil1end, soil temperature (1 cm depth) at the end of the experiment; Tsoil1start, soiltemperature (1 cm depth) at start of the experiment; Tsoil10end, soil temperature(10 cm depth) at the end of the experiment; Tsoil10start, soil temperature (10 cmdepth) at start of the experiment.


The strong intercorrelation of most of the variables causes a very low conditional

effect of 15 of 17 parameters, but eight of them, including air, faecal and soil

temperature, have a statistically significant effect.

The two periods of highest flight activity are analysed separately (10:00–14:00 h:

figure 6; 18:00–22:00 h: figure 7) to identify possible correlations between micro-

climate and abundance of guilds at a higher temporal resolution.10:00–14:00 h. During their peak flight period telecoprids show no close

correlation with any microclimatic parameter, and only a slightly positive

correlation with the air temperature at the end of the exposure period (i.e.

during the collecting time). The abundance of their kleptoparasites, however, is

related to all absolute temperatures. Absolute numbers of paracoprids are related

to a lower increase of soil temperature. The most important parameters that can

affect guild structure are the temperature of the soil in 1 cm depth at the end of

the exposure period, the relative air humidity and the soil temperatures in 10 cm

depth. However, only the soil temperature in 1 cm depth at the end of the expo-

sure period and the air temperature at 10:00 h have a significant effect in the

interplay of all variables (table 5).18:00–22:00 h. Around dusk the endocoprids and the kleptoparasites of para-

coprids have their single peak (figure 3). They are not closely correlated with any

of the environmental parameters that we measured. Endocoprids may prefer a

higher air temperature. The paracoprids, however, are strongly positively corre-

lated with all absolute temperatures and negatively correlated with relative air

humidity. Most of these parameters are possibly affecting the guild structure

(table 6). Only the relative air humidity at 22:00 h is negligibly correlated which

approximates to saturation at every night in the rainy season (table 3). In the

Table 4. Eigenvalues of the environmental variables in the RDA (all samples considered).

Marginal effects Conditional effects

Variable l1 Variable lA P

Tair end 0.46 Tair end 0.46 0.001Tsoil1end 0.46 18:00–22:00 h 0.20 0.001Tfaeces 0.45 RHend 0.03 0.001Rhend 0.40 22:00–2:00 h 0.04 0.001diffTsoil10 0.36 6:00–10:00 h 0.02 0.001Tsoil10end 0.33 Tfaeces 0.03 0.00110:00–14:00 h 0.32 Tsoil10end 0.01 0.020diffTair 0.28 diffTair 0.00 0.02618:00–22:00 h 0.26 14:00–18:00 h 0.01 0.010diffTsoil1 0.18 Tsoil1start 0.01 0.350Tsoil1start 0.14 Tair start 0.00 0.49322:00–2:00 h 0.14 2:00–6:00 h 0.00 0.371Rhstart 0.11 Tsoil1end 0.00 0.531Tair start 0.11 diffTsoil1 0.00 0.6572:00–6:00 h 0.07 Tsoil10start 0.00 0.79914:00–18:00 h 0.04 diffTsoil10 0.01 0.891Tsoil10start 0.04 RHstart 0.00 0.6836:00–10:00 h 0.02

The significance of the variables is tested by a Monte Carlo Permutation Test (Canoco;999 permutations).

For abbreviations see figure 5.


interplay of all microclimatic variables, only the soil temperature in 10 cm depth

at 18:00 h has a major and significant effect, whereas the effects of air tempera-

ture are significant but only minor (table 6).

Differences to previous results

The number of the kleptoparasites of telecoprids is remarkably lower than in

our habitat experiment (Krell et al., 2003) where we exposed the dung in the

savanna from 6:00 h to 16:00 h. We suppose that the number of kleptoparasites

is correlated with the length of deposition time during the activity period of these

beetles. They are likely to accumulate in the dung pat during the day, because the

number of arriving individuals is higher than the number of successful individuals

leaving the pat with their host.

FIG. 6. RDA ordination triplot of samples, guilds and environmental variables, based onlog-transformed guild abundance data of the period 10:00–14:00 h (15 samples).Vectors of endocoprids and kleptoparasites of paracoprids are removed becauseof their low abundance (see table 1). Eigenvalues: axis 1, 0.488; axis 2, 0.164. Forabbreviations see figure 5.


Discussion

Diel separation of coprophagous guilds

Habitat heterogeneity generally increases species diversity by enabling species

that are competitively inferior in one habitat to be competitively superior in

another. This heterogeneity may be spatial or temporal (Southwood, 1978; Tokeshi,

1999: 294). Because of a completely different microclimate at night and daytime,

the same habitat can be considered to exist in two different states. In the

forest–savanna mosaic this diel heterogeneity is most distinctive within open

habitats (Krell et al., 2003). In tropical ecosystems, species composition of diurnal

and nocturnal dung beetle assemblages are clearly different (Hanski and

Cambefort, 1991), particularly in open habitats (Cambefort and Walter, 1991).

In a parallel study, we found that competitively inferior dung beetle guilds were

less abundant in habitats where the competitively superior guilds predominate

(Krell et al., 2003). In the savanna parkland, this spatial separation of guilds has

FIG. 7. RDA ordination triplot of samples, guilds and environmental variables, based onlog-transformed guild abundance data of the period 18:00–22:00 h (15 samples).Vectors of telecoprids and their kleptoparasites are removed because of their lowabundance (see table 1). Eigenvalues: axis 1, 0.478; axis 2, 0.303. For abbreviations seefigure 5.


its temporal parallel at a diel level: the competitively most inferior endocoprids

are flying to the resource in large numbers only around dusk when the best

competitors, the telecoprids, are not active. Walter (1985) described a similar

pattern from central Africa. Telecoprids generally prefer fresh dung without crust

to make their balls. Dung pats exposed before dusk might be already too old or less

attractive for telecoprids when their next activity period starts. Around dusk, we

found also the highest abundance of the competitively intermediate paracoprids.

Paracoprids, however, do not always use the dung completely (figure 2) so that

endocoprids have a chance to feed and reproduce in dung pats used by paracoprids.

Table 6. Eigenvalues of the environmental variables in the RDA of the samples of theperiod 18:00–22:00 h.



Tsoil10start 0.40 Tsoil10start 0.40 0.001diffTsoil1 0.36 diffTair 0.14 0.015Tsoil1start 0.36 RHend 0.07 0.117Tsoil10end 0.35 Tair end 0.12 0.011diffTair 0.35 Tair start 0.07 0.031Tfaeces 0.32 diffTsoil1 0.04 0.094Tsoil1end 0.31 RHstart 0.03 0.231Tair start 0.29 Tsoil1start 0.02 0.355Rhstart 0.24 Tsoil10end 0.02 0.600Tair end 0.22 Tfaeces 0.03 0.115diffTsoil10 0.17 diffTsoil10 0.03 0.153Rhend 0.08 Tsoil1end 0.00 0.731



Table 5. Eigenvalues of the environmental variables in the RDA of the samples of theperiod 10:00–14:00 h.



Tsoil1end 0.32 Tsoil1end 0.32 0.001Rhend 0.31 RHend 0.11 0.054Tsoil10start 0.27 Tair start 0.15 0.010Tsoil10end 0.23 Tair end 0.04 0.322Rhstart 0.21 Tsoil10start 0.03 0.497Tair start 0.19 Tsoil10end 0.03 0.541diffTsoil1 0.18 Tfaeces 0.02 0.710Tair end 0.16 Tsoil1start 0.02 0.624Tfaeces 0.16 diffTsoil10 0.04 0.481Tsoil1start 0.13 diffTsoil1 0.03 0.607diffTair 0.06diffTsoil10 0.04




As between habitats (Krell et al., 2003) we find a diel separation of competitors

at the guild level.

Abundance peaks and discontinuous competitive level

During the night and in the morning (22:00–10:00 h) the overall abundance of

dung beetles is very low and certainly at a non-competitive level at the resource

(figure 3). Inferior competitors would therefore have had the chance to use the

resource extensively during this time of the day, but they did not.

We may slightly underestimate the utilization of the resource between 22:00 h

and dawn, because the number of Coprini and Heliocopris spp. (big tunnellers)

was very low during the study period, presumably because the rainfall during

the first half of the rainy season was much below average and Coprini emerge

mainly after strong rain. In a preliminary study at the same site in 1996 (a

relatively wet year) we had a much higher number of Coprini in our samples,

some of which came to the dung after 23:00 h (Westerwalbesloh, unpublished

data). Many Coprini are known to have a flight period that is extended until

long after dusk (Walter, 1985; Davis, 1999; personal observation), so they are

able to use the resource during a period without any competitive pressure.

However, they are not very abundant then (Davis, 1999; Westerwalbesloh,

unpublished data) and use only a part of the resource. The greater part (or,

in our study, nearly all) of the resource remains unused between 22:00 h and

dawn.

We assume that the activity peaks of dung beetles are not correlated with the

availability of dung because herbivore dung appears as an available resource all day

long: buffaloes defecate randomly (Leuthold, 1977: 32), there seem to be no diel

preference periods (Mloszewski, 1983: 120).

Our results indicate that there are vacant temporal refuges (Tokeshi, 1999: 303)

of which dung beetles cannot take advantage whether they are competitively

superior or inferior. Remmert (1976) did not know any well-analysed example of

an ecological niche that is available all the day but realized only during a certain

period of the day. The diel activity of savanna dung beetles is such an example.

Why is the dung beetle abundance so unequally distributed over the day with peaks

of high competition and periods when the resource is neglected?

Neglecting resources due to physiological constraints?

The abundance peak at dusk is a global pattern, and we often find the diurnal

peak around midday (Peck and Forsyth, 1982; Walter, 1985; Fincher et al., 1986;

Davis, 1996; Davis, 1999; Feer, 2000). The nocturnal abundance minimum between

22:00 h and just before dawn is also present in temperate regions (Koskela, 1979),

in Borneo (Davis, 1999), South Africa (Davis, 1996), less pronounced in

South America (Feer, 2000) and postponed to after 2:00 h in Kenya (Heinrich

and Bartholomew, 1979). According to Walter (1985), Afrotropical dung beetles

show flight activity throughout the whole day, but he does not give the abundance

data of the species per hour. Therefore, it is not clear when the species have their

activity peaks. Since the activity generally starts and ends with a low number

of active beetles (Carne, 1956; Koskela, 1979; Palmer and Garcıa Ple, 1992), an

undefinable part of the activity time indicated by Walter may be due to singletons

alone.


Using light intensity as activity trigger probably leads to the crepuscular activ-

ity peak. The abundance peak at dusk is most likely to be caused by a mechan-

ism to synchronize the flight by light intensity differences. Light intensity was

found several times to be responsible for the onset of flight of crepuscular dung

beetles (Aphodius: Carne, 1956; Landin, 1968: 23; Onitis: Houston and McIntyre,

1985) and also in other Scarabaeidae (Kosmachevskii, 1941; Wensler, 1974).

Light intensity possibly functions only as a fine trigger near the flight period

(Carne, 1956) or as a trigger for emergence with an endogenous circadian clock

eventually inducing the onset of flight (Evans and Gyrisco, 1958), because the

activity rhythm can be completely determined by an endogenous clock, but

activity can be prohibited by too much light (Vico et al., 1986). Since light

intensity changes regularly and periodically only at dusk and dawn, species that

use this factor for regulation (i.e. synchronization) of their activity periods have

to be crepuscular. They are able to approach the resource only during a very

limited period of the day and can, consequently, use only a limited number of

the resource patches that are daily deposited in their activity range: only those

that are deposited just before or during their flight period. This habit is certainly

a trade-off between the advantage of the ease of finding a sexual partner (by

synchronization of flight periods) and the disadvantage of a restriction of the

use of resources. A longer activity period with more possibilities to use newly

appeared resources seems to be less advantageous than temporally limited flight

activity.Paracoprids show a positive correlation with temperature of faeces, soil and air

during their activity peaks at dusk (figure 7), but a negative correlation with all

temperature parameters during their diurnal peak (figure 6). They seem to avoid

high diurnal temperatures, which may probably lead to lethal body temperatures

particularly in large black beetles flying in the sun at midday. Lethal body

temperatures for insects are between 40 and 50‡C. A big dung beetle may already

be 44‡C at take-off (Bartholomew and Heinrich, 1978). The competitive superiority

of thermophilous telecoprids is unlikely to be the reason for this pattern, because

their abundance is not negatively correlated with the number of paracoprids during

their activity peak (figure 6).

Since crepuscular paracoprids are positively correlated with temperature

parameters during their activity peak (figure 7), their low number at dawn is as

expected: although dawn is as suitable as dusk for synchronizing flight activity, late

night and dawn are the coldest hours of the day (table 3).Correlation of guild abundance and temperature: the inevitability of a midday

peak. A positive correlation of temperature with flight activity of dung beetles

has been shown in the paracoprid Onitis alexis (Houston and McIntyre, 1985:

soil temperature in 3 cm depth) and in Aphodius (Carne, 1956: air temperature).

Martın-Piera et al. (1994) found that the diurnal Palaearctic roller Sisyphus

schaefferi (L.) is active all day and night if the temperature is at least 29‡C. In

a parallel study comparing habitat types, we found a positive correlation

between abundance of endocoprids, telecoprids and their kleptoparasites with

temperature (Krell et al., 2003). From the present study also a positive correla-

tion between temperature and the abundance of paracoprids, telecoprids and

their kleptoparasites results, if we pool the samples from all over the day

(figure 5). As in the habitat study, numbers of telecoprids and their kleptopara-

sites are strongly correlated with dung, soil and air temperatures at the end of


the exposure period (i.e. when the temperatures have their maximum). This cor-

roborates our former hypothesis (Krell et al., 2003), that telecoprids prefer

higher temperatures to perform their energetically costly rolling behaviour effec-

tively. Bartholomew and Heinrich (1978) found that the velocity of beetles

increases with the body temperature. For the success of the kleptoparasites of

rollers, high temperature is likely to be only indirectly necessary by increasing

the number of telecoprid hosts.For the (diurnal) telecoprids it seems only to be crucial to have their activity

period during the warmest time of the day. It does not matter how warm it is,

because their numbers show no correlation with any temperature parameter during

their activity peak (figure 6) (or the sample size is too low to show any such

patterns).

Summary

‘Temporal partitioning is, in theory, even less likely. No energetic gain can be

derived from not feeding during most time periods…’ This consideration of

Schoener (1986) does not apply if organisms are forced to a limited activity period

by energetic constraints or at least temporal energetic optima. The diel activity

peaks of dung beetles depend on the climatic optima for the most abundant groups:

the competitively superior telecoprids have their peak at midday when maximum

heat enables them to perform their energetically costly rolling behaviour at the

highest possible speed. The competitively intermediate paracoprids and the com-

petitively inferior endocoprids have their peak around dusk (1) when they can easily

synchronize their flight activity using light intensity changes and (2) when the

superior competitors are not active. During these two activity peaks at midday and

around dusk, the abundance of dung beetles at the resource is very high, causing

to a certain degree obvious competition. On the other hand, between 22:00 h and

10:00 h the resource is hardly used and would offer inferior competitors good

opportunities. However, shifting or prolonging their flight periods to other times

of the day is not a realized strategy to avoid competition. This is probably due to

physiological constraints: the need for high optimum temperature and dependence

on light intensity patterns, respectively.

AcknowledgementsOur employees in the Lola Camp, Koffi Kouadjo, Lakado, Abdoulaye Dabila

Kouadjo and the late Adoulae Ada created a pleasant environment for living and

working in the field. We thank Paul Eggleton and Dorothy Newman, The Natural

History Museum London, for helpful comments. The study was supported by a

grant of the Deutsche Forschungsgemeinschaft (DFG) (Li 150/18-1,2,3, K.E.L.)

and was initially a part of the DFG programme ‘Mechanismen der Aufrechter-

haltung tropischer Diversitat’. Fieldwork was permitted by the Ministere de

l’Agriculture et des Ressources Animales de Cote d’Ivoire, Abidjan.

Appendix

Numbers of individuals per guild per sample

Sample numbers are as written on the specimen labels; Klepto.Para. are

the kleptoparasites of paracoprids; Klepto.Tele. are the kleptoparasites of

telecoprids.


2:00–6:00 h

Sample no. SC20 SC21 SC22 SC44 SC45 SC46 SC55 SC56 SC57 SC58 SC84 SC85 SC86 SC87 SC88

Total Mean SDDate ofcollection

26May

26May

26May

5June

5June

5June

8June

8June

8June

8June

11July

11July

11July

12July

12July

Endocoprids 0 3 5 6 2 7 6 5 6 3 2 0 0 4 2 51 3.4 2.38Paracoprids 44 30 40 40 56 130 27 28 28 28 28 67 46 21 41 654 43.6 26.93Telecoprids 3 3 2 0 2 3 4 6 5 6 0 0 0 0 0 34 2.3 2.25Klepto.Para. 0 1 0 2 1 0 1 0 1 1 1 1 1 0 2 12 0.8 0.68Klepto.Tele. 12 5 8 1 0 1 1 3 2 3 1 0 1 1 0 39 2.6 3.38Total 59 42 55 49 61 141 39 42 42 41 32 68 48 26 45 790 52.7 26.79

6:00–10:00 h



8May

8May

8May

28May

28May

28May

8June

8June

8June

8June

12June

12June

12June

12July

12July

Endocoprids 0 1 1 1 3 3 1 0 0 1 1 6 4 6 3 31 2.1 2.02Paracoprids 50 31 67 19 20 28 34 23 57 63 34 22 72 25 34 579 38.6 18.23Telecoprids 49 21 79 1 0 2 130 54 152 113 28 78 288 2 0 997 66.5 79.43Klepto.Para. 0 0 0 4 7 4 0 0 0 0 1 2 1 1 3 23 1.5 2.10Klepto.Tele. 0 1 1 26 63 59 10 13 82 63 14 22 148 3 8 513 34.2 41.58Total 99 54 148 51 93 96 175 90 291 240 78 130 513 37 48 2 143 142.9 125.29

22

44

S.

Krell-W

esterwa

lbeslo

het

al.

10:00–14:00 h



18May

18May

18May

18May

30May

30May

30May

30May

7June

7June

7June

7June

10June

10June

10June

Endocoprids 0 0 0 2 0 0 0 0 0 0 0 0 0 2 0 4 0.3 0.70Paracoprids 140 148 90 231 125 239 89 154 140 246 165 192 223 207 129 2 514 167.6 51.95Telecoprids 460 445 369 463 781 1 427 799 730 360 728 377 368 578 402 272 8 559 570.6 292.87Klepto.Para. 0 2 0 0 0 0 0 0 0 0 0 0 0 1 0 3 0.2 0.56Klepto.Tele. 59 97 81 251 107 49 109 225 41 107 79 83 14 27 19 1 348 89.9 68.25Total 659 692 540 947 1 013 1 715 997 1 109 541 1 081 621 643 815 635 420 12 428 828.5 327.33

14:00–18:00 h



7May

7May

7May

7May

27May

27May

6June

6June

6June

6June

9June

9June

9June

8July

8July

Endocoprids 0 0 3 0 2 1 5 2 2 3 6 7 2 23 22 78 5.2 7.33Paracoprids 63 90 93 52 66 85 30 59 44 70 139 116 116 50 102 1 176 78.4 30.87Telecoprids 8 31 57 26 88 0 71 93 32 71 197 156 158 112 143 1 243 82.9 60.09Klepto.Para. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0.0 0.00Klepto.Tele. 0 0 0 0 119 48 10 13 6 81 38 21 72 254 568 1 230 82.0 150.40Total 71 121 154 78 275 134 116 167 84 225 380 300 348 438 835 3 727 248.5 200.27

Diel

sepa

ratio

no

fd

un

gb

eetleg

uild

s2

24

5

18:00–22:00 h



13May

13May

24May

24May

27May

27May

27May

4June

4June

4June

9June

9June

9June

23June

23June

Endocoprids 97 8 340 206 106 86 43 90 147 166 70 88 88 115 145 1 795 119.7 77.96Paracoprids 755 393 664 928 163 184 182 247 294 256 71 109 86 12 18 4 362 290.8 278.95Telecoprids 1 0 6 4 3 1 0 1 0 6 0 0 0 0 0 22 1.5 2.20Klepto.Para. 1 0 8 17 16 4 13 16 17 15 17 24 38 6 5 197 13.1 9.81Klepto.Tele. 3 2 16 11 7 2 4 3 3 0 1 1 1 2 0 56 3.7 4.43Total 857 403 1 034 1 166 295 277 242 357 461 443 159 222 213 135 168 6 432 428.8 373.36

22:00–2:00 h



25May

25May

25May

25May

3June

3June

3June

3June

5June

5June

24June

24June

24June

10July

10July

Endocoprids 1 4 8 13 10 11 5 9 39 15 15 8 15 15 4 172 11.5 8.89Paracoprids 8 16 3 7 11 17 10 6 13 5 1 1 4 13 5 114 7.6 4.69Telecoprids 2 3 2 5 5 6 7 9 0 1 0 0 0 4 1 45 3.0 2.88Klepto.Para. 0 0 0 1 0 0 0 0 0 0 0 0 0 1 0 2 0.1 0.35Klepto.Tele. 1 0 0 0 2 2 6 3 1 0 0 1 0 5 1 22 1.5 1.88Total 12 17 13 26 28 36 28 27 53 21 16 10 19 38 11 355 23.7 11.96

22

46

S.

Krell-W

esterwa

lbeslo

het

al.

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Diel separation of Afrotropical dung beetle guilds - avoiding competition and neglecting resources

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