Roles of endothermy in niche differentiation for ball-rolling dung beetles (Coleoptera:...

© 2007 The Authors544 Journal compilation © 2007 The Royal Entomological Society

Ecological Entomology (2007), 32, 544–551

Introduction

Heinrich (1993) defines thermoregulation as ‘the maintenance of a specific body temperature (or temperature range) independ-ent of passive processes, such as radiation, convection, evapora-tion, and the body’s metabolism during different activities’. Thermoregulation is often closely related to the internal func-tioning of an insect but is also affected by its relationship with its environment.

Temporal and spatial activity patterns are influenced by ther-moregulation strategy. In desert tenebrionids, thermally induced shifts in activity patterns allow different species to divide up a wide range of habitats and subsequently these diverse patterns

suggest a possible adaptation that may reduce interspecific competition ( Holm & Edney, 1973; Hamilton, 1975 ). In sub-tropical ants, the observed pattern is a general trade-off between behavioural dominance and thermal tolerance ( Bestelmeyer, 2000 ).

The daily activity of ectotherms is generally determined by day length, while many endothermic species show vespertine, crepuscular, or nocturnal activity ( Corbet, 1963; Heinrich, 1993 ). For example, in Micrathyria dragonflies, larger species can shift their major activity peaks to early or late in the day, reducing competitive interactions with smaller species that are restricted to midday ( May, 1985 ). In Scarabaeus , various mech-anisms for thermoregulation may explain how closely related sympatric species respond to environmental temperature, and how this favours their coexistence ( Verdú et al. , 2004 ). In some stingless bees, thermoregulatory differences related to body size

Correspondence: José R. Verdú, Instituto de Biodiversidad CIBIO, Universidad de Alicante, E-03080 Alicante, Spain. E-mail: [email protected]

Roles of endothermy in niche differentiation for ball-rolling dung beetles (Coleoptera: Scarabaeidae) along an altitudinal gradient

J O S É R . V E R D Ú 1 , L U C R E C I A A R E L L A N O 2 , C AT H E R I N E N U M A 1 a n d E S T E FA N Í A M I C Ó 1 1 Instituto de Biodiversidad CIBIO, Universidad de Alicante, Alicante, Spain and

2 Departamento de Biodiversidad y Ecología Animal, Instituto de Ecología, A.C., Apartado Postal 63, Veracruz, Mexico

Abstract . 1. An analysis of whether niche differentiation in ball-rolling dung beetles can be explained by the way in which they regulate their body temperature was conducted.

2. A priori assumptions were: (i) if thermoregulation affects niche partitioning, sympatric species must have different endothermic strategies that minimise encounters; or, alternatively (ii) if two co-occurring species show the same thermoregulation pattern and their flight periods overlap, they might be avoiding competition by exhibiting different resource preferences or different food relocation behaviour.

3. The ball-rolling dung beetles studied showed a hierarchical structure based on the species’ endothermic capacity, measured as temperature excess [ T ex = difference between body temperature ( T b ) and ambient temperature ( T a )]. Those with a high T ex (10 – 15 °C) were located exclusively at altitudes >1000 m a.s.l. On the coastal plains, species with a high T ex were restricted to flying at night when the T a was lower. Species with a lower T ex (less than 10 °C higher than T a ) were found in the coastal plains zone.

4. Where there was sympatry with similar trophic habits, the species involved showed very different thermal niches, and where there was significant overlap of thermal niches between sympatric species, trophic habits of species were very different.

5. The results suggest that it is possible to use the concept of the thermal niche as a tool to explain interspecific interactions and the spatial distribution of species.

Key words . Ecophysiology , niche overlap , null models , thermal niche , thermoregula-tion , Scarabaeoidea .

Thermal niche differentiation in dung beetles 545

© 2007 The AuthorsJournal compilation © 2007 The Royal Entomological Society, Ecological Entomology, 32, 544–551

and coloration suggests niche differentiation and different bio-geographic distributions at the interspecific level ( Pereboom & Biesmeijer, 2003 ). Thus, thermoregulation may broaden a thermal niche in both space and time ( May, 1985 ).

Dung beetles are good fliers and usually approach a food source during flight. Dung is an ephemeral resource and the beetles that arrive at fresh dung first, consume, bury, and dis-perse it quickly. The quality of this food resource decreases over time so it is less attractive to the beetles that arrive later ( Heinrich & Bartholomew, 1979 ). However, coprophagous scarab beetles use their substrate in different ways, by which they are classi-fied into guilds (e.g. Halffter & Edmonds, 1982 ). 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. In rollers, it has been demonstrated that endothermy is directly related not only to walking and flight but also to ball making and ball rolling; the latter being the essence of scramble compe-tition ( Bartholomew & Heinrich, 1978; Heinrich, 1993; Ybarrondo & Heinrich, 1996 ).

Resource partitioning and competition have doubtless con-tributed to the evolution of breeding and flight behaviours, and the thermoregulation strategies that favour intraspecific interac-tions over interspecific ones among sympatric species of dung beetles ( Caveney et al. , 1995; Ybarrondo & Heinrich, 1996; Verdú et al. , 2004 ). Food relocation is a key characteristic of adult behaviour in dung beetles and it is accomplished by pack-ing pieces of dung into a tunnel dug by the beetle (tunnellers), or by removing a portion of dung from the mass, rolling it some distance away from the source and then depositing or burying it (rollers) ( Halffter & Edmonds, 1982 ). The dung beetles of a given community tend to be quite exact in the timing of their daily activities ( Halffter & Matthews, 1966; Fincher et al. , 1971; Mena et al. , 1989; Caveney et al. , 1995 ). From a resource parti-tioning viewpoint, the type and size of the resource, the size of dung beetles, habitat selection, and temporal activity can be col-lapsed into two composite dimensions: for example the size of dung beetles related to daily activity, and resource selection re-lated to seasonality ( Hanski & Cambefort, 1991 ). Both daily activity and seasonality are strongly related to the thermal biol-ogy of dung beetles (e.g. Bartholomew & Heinrich, 1978; Verdú et al. , 2004, 2006 ). In some situations, competition is severe and undoubtedly greatly influences the structure of the communities ( Hanski & Cambefort, 1991 ). For the rollers, in particular, there are many observations of direct interference competition be-tween species (individuals attempting to steal dung balls from one another) (see Halffter & Matthews, 1966 ).

The main objective of this study is to establish whether niche differentiation between some dung beetles can be explained by thermoregulation patterns. Temperature excess ( T ex ), measured as the difference between body temperature ( T b ) and ambient temperature ( T a ), was used applied to endothermy. To test the importance of thermoregulation patterns on niche differentia-tion, all of the species of endothermic roller dung beetles inhab-iting an altitudinal gradient comprising three different landscapes in Veracruz, Mexico were studied. Hence, the assumptions were: (i) if thermoregulation affects niche partitioning, sympat-ric species must have different endothermic strategies that mini-

mise encounters; or, alternatively (ii) if two co-occurring species show the same thermoregulation pattern (thermal niche) and their flight periods overlap, they might be avoiding competition by exhibiting different resource preferences or different food relocation behaviour. The latter explanation can be rejected a priori because all of the dung beetles studied are rollers.

Materials and methods

Study area

The dung beetles studied were distributed throughout three landscapes (for details, see Fig. 1 and Table 1 ) in the central re-gion of the state of Veracruz, Mexico (19°26 � 39 ″ – 19°38 � 45 ″ N, 96°35 � 18 ″ – 97°09 � 54 ″ W). These were (i) tropical landscape, (ii) intermediate landscape, and (iii) mountainous landscape. The vegetation of the coastal plains (<1000 m a.s.l.) is characterised by mangroves, deciduous forest on the more elevated terrain, tropical oak forests, and medium semi-deciduous forest in the most humid ravines. Mean annual temperature ranges from 22.3 to 24.5 °C and total annual precipitation is 1500 – 2000 mm ( Castillo-Campos, 1985, 1991; Acosta, 1986; Robles, 1986; Cházaro-Basáñez, 1992 ). The intermediate landscape (1000 – 2000 m a.s.l.) is characterised by oak forest, tropical montane cloud forest and pine – oak forest. Mean annual temperature is 12.3 – 22.3 °C and total annual precipitation is 1200 – 2500 mm ( Narave, 1985; Castillo-Campos, 1991; Zamora, 1992 ). The mountainous landscape (>2000 m a.s.l.) is characterised by pine forest, fir forest and mountain pastures. Mean annual temperature is 11.0 – 12.9 °C and total annual precipitation is 800 – 1500 mm ( Narave, 1985 ).

Body and ambient temperature measurements

The thermal biology of eight Scarabaeinae species distributed throughout the three landscapes was studied ( Table 1 ). Six of them were sympatric species.

The species studied are active mainly from June to November ( Arellano, 1992; Díaz, 1998; Halffter & Arellano, 2001, 2002 ; J. R. Verdú, pers. obs.), and this was considered the ideal period to test flight activity and thermoregulation in the field. All meas-urements of body temperature and climatic conditions were made from 17 July to 18 November 2000 (over 115 sampling days).

For coprophagous forest species, four piles of bait (two of cow dung and two of human excrement) were placed on the forest soil inside circular areas of soil (diameter = 1 m) surrounded by solid plastic fences (height = 20 cm) that did not hinder the dis-persion of odour. For necrophagous forest species, two dead hens were placed inside different circular plastic fences. These fences allowed live individuals of different species to be found.

For coprophagous open site species 10 piles (around 1 kg) of cow dung, separated by 25 m, were placed in the pastures. For diurnal beetles, measurements and observations at the study sites were made from 07.00 hours until the beginning of sunset (ca 19.00 hours). For Canthon humectus only, the period was

546 José R. Verdú et al.


reduced (from 07.00 until 16.00 hours) because of the extremely cold temperatures in the mountain zone. For crepuscular and nocturnal species the period began at the beginning of sunset (dusk) and continued until 2 h after the last record had been obtained (approximately 03:00 hours).

Body temperature ( T b ) was measured with Ni-Cr ( + )/Ni-Al ( – ) Type K thermocouples (THERMOCOAX ™ ; Thermocoax, Suresnes, France) threaded into hypodermic needles (0.25 mm

in diameter). Intrinsic response time of thermocouples was 7 ms and mean sensitivity 41 � V °C – 1 . Temperatures were read using MMS3000-T4 ™ Multi Measurement System ™ (Commtest Instruments, Knoxville, Tennessee), with an accuracy of 0.5 °C. To obtain body temperature, the thermocouple was inserted into the centre of the metathorax. In order to obtain a complete range of flight activity for each species, the authors arrived in the field 2 h before the beetles became active and left 2 h after the last

Fig. 1. The elevational gradient studied in the central region of the state of Veracruz, Mexico. Asterisks indicate sampling areas for thermoregulation records for each eleva-tional landscape. White circles (regular sam-pling sites) and triangles (complimentary sampling sites) indicate locations with pres-ence data on dung beetles distribution from Arellano (1992), Halffter et al. (1995) and Halffter and Arellano (2001, 2002) .

Table 1. The altitudinal range and general characteristics of the eight Mexican roller dung beetle species studied.

Species Functional group Altitudinal range (m a.s.l.) Habitat Body size (mm) Body mass (g)

Canthon cyanellus Le Conte (1859) N – D 200 – 500 F – E 10.18 ± 0.98 0.064 ± 0.020 Canthon femoralis (Chevrolat, 1834) C – D 200 – 400 F 8.80 ± 0.75 0.025 ± 0.003 Canthon humectus (Say, 1832) C – D 1700 – 2200 P 14.22 ± 1.04 0.20 ± 0.06 Canthon indigaceus chevrolati Harold (1868)

C – D 200 – 500 P 13.87 ± 0.87 0.06 ± 0.02

Deltochilum lobipes Bates (1887) N – No 200 – 400 F 27.64 ± 1.25 0.86 ± 0.29 Deltochilum mexicanum Burmeister (1848)

N – No 1400 – 1800 F – E 21.0 ± 1.1 0.54 ± 011

Deltochilum pseudoparile Paulian (1938)

C – Crep 200 – 400 F 15.77 ± 0.85 0.10 ± 0.02

Deltochilum scabriusculum Bates (1887)

C – No 200 – 500 F 27.01 ± 1.3 0.84 ± 0.17

Abbreviations: C, coprophagous; N, necrophagous; D, diurnal; No, nocturnal; Crep, crepuscular; P, pasture; F, forest; E, forest edge.



observation. All temperatures, including ambient temperature during flight ( T a ), were recorded within 1 – 3 s of capture and latex dissection gloves were used to protect the beetles from heat transfer. A total of 166 measurements of body tempera-ture were obtained in the field. In addition, 21 measurements were recorded in climate chambers under laboratory condi-tions varying the environmental temperature from 15 to 40 °C. The species studied were released into the climate chambers and the researchers waited for the beetles to fly. The beetles were then captured by hand when they landed (using latex dissection gloves) and a thermocouple was inserted in the mesothorax.

Data analysis

The Czekanowski index for each pair of species ( Feinsinger et al. , 1981 ) was calculated to quantify patterns of niche overlap between species:

O O p pi i

i

n

12 21 1 21

1.0 0.5= = − −=∑

where p 1 i is the fraction of flight observations for species 1 that occurred in resource state i. For the analyses of thermal niche overlap, the resource states represent the different classes of sur-rounding temperature. Thus, the index approaches 0 for species that never coincide in flight at the same T a , and is 1.0 for pairs of species that fly in an identical T a range. Afterwards, a cluster analysis was carried out using Ward’s linkage rule.

To test the statistical significance of thermal niche overlap, a null model analysis was used. In this model the observed data were randomised among species. Species (in rows) and T a classes (in columns) were used to construct the matrix. To test for non-random thermal niche overlap patterns, three different randomisation algorithms (RA) were used ( Winemiller & Pianka, 1990; Albrecht & Gotelli, 2001 ). The first algorithm (RA 2 ) retains the zero structure of the matrix. This is recom-mended when certain resource states are unavailable for certain species (such as T a in the present study). The second algorithm (RA 3 ), the scrambled-zeros randomisation algorithm, retains observed data but randomly relocates them among all possible resource states, so the zero structure of the matrix is not re-tained. The third algorithm (RA 4 ) retains both observed niche breadth and the zero structure of the observed matrix ( Winemiller & Pianka, 1990 ). The assumption recommended by Schoener (1974) that ‘observed niche overlaps are less than expected by chance’ was applied. In the absence of thermal niche overlap, high variance in the surrounding temperature while the beetle is flying might indicate internal guild structure in which some species pairs have very similar temperature requirements for flying while those of others are very dissimilar ( Winemiller & Pianka, 1990 ). ecosim 7.0 software ( Acquired Intelligence Inc., & Kesey-Bear, Burlington, VT, U.S.A. - see Gotelli & Entsminger, 2003 ) was used for all null model analyses.

To determine if there were any significant differences between the classes of T a range tolerated by species, a one-way anova with the Fisher protected least significant difference (PLSD) post

hoc test for pairwise comparisons was used; the data having been tested for normality and homogeneity of variances. statistica software ( StatSoft Inc., 1997 ) was used for these analyses.

Results

Thermal niche overlap

Species flight distributions are clearly separated with respect to T a ( Fig. 2 ). Minimum values of 16.7 °C in the T a range were ob-served for C. humectus , a diurnal species of the high plateau com-mon to open mountain sites, and maximum values of 33.2 °C in Canthon indigaceus , a diurnal species of open tropical sites. All species studied display well-defined specific ranges for T b that does not seem to be influenced by the T a ( Fig. 3 ). Thus, from a thermoregulation point of view the spatio-temporal distribution of species are clearly separated with respect to T a ( Fig. 3 ). In the RA 2 and RA 4 models ( Table 2 ), observed thermal niche overlap was less than expected by chance, but not significantly different ( P = 0.12 and P = 0.29 respectively). Only the unrestricted analysis (RA 3 ) showed a tendency towards thermal niche overlap greater than expected by chance but this was not statistically significant ( P = 0.18). Variance in thermal niche overlap, however, differs sig-nificantly from the expected ( P < 0.05). According to Winemiller and Pianka (1990) observations, the high variance observed in the present study indicates the existence of a guild structure in which some species display great similarities and others are very differ-ent ( Fig. 4 ). The pairwise Czechanowski index ( O ) and anovas showed, in general, little thermal niche overlap and only two re-sults with no significant difference in T a between sympatric spe-cies. In this sense, the only pairs of species with a significant, high degree of thermal niche overlap were Canthon femoralis and C. cyanellus ( O = 0.676; Fisher PLSD = 0.75; d.f. = 7; P < 0.05), as well as Deltochilum lobipes and D. scabriusculum ( O = 0.680; Fisher PLSD = 0.81; d.f. = 7; P < 0.05). Regarding the existence of a guild structure, cluster analysis ( Fig. 4 ) revealed two main groups characterised by both ‘Nearctic or Neotropical nocturnal’ and ‘Neotropical diurnal (or crepuscular)’ rollers (see also Table 1 ). Within the first group, one species was representative of the mountain landscape ( C. humectus ), one was representative of the intermediate landscape ( Deltochilum mexicanum ), and two were nocturnal species from the coastal plains ( D. lobipes and D. scabriusculum ). In this group, only one species from the open lowlands ( C. humectus ) was separated from the forest species group ( D. mexicanum , D. lobipes , and D. scabriusculum ). A second group consisted of all diurnal species from the coastal plains (with the exception of Deltochilum pseudoparile , which is considered a crepuscular species). In this group, the only species from open lowlands ( C. indigaceus ) was separated from the forest species group ( C. cyanellus , C. femoralis and D. pseudoparile ).

Discussion

Different thermoregulation patterns between sympatric species of dung beetle favour the coexistence of species and preclude interspecific competition ( Bartholomew & Heinrich, 1978;



Caveney et al. , 1995; Verdú et al. , 2004 ). The altitudinal gradi-ent studied was a good stage suitable for analysing the relation-ship between the types of thermoregulation and spatial and temporal segregation of sympatric species with similar ecologi-cal requirements. The Canthonina species studied shows a hier-archical structure based on their endothermic capacity. Species with a high T ex (10 – 15 °C) were located exclusively in the high and transition mountain landscapes (>1000 m a.s.l.) ( Fig. 3 and Table 1 ). On the coastal plains, the species with a high T ex have the option of flying at night when the T a is lower. The other spe-cies with a lower T ex (below 10 °C) were sympatric and restricted to the coastal plains zone.

A guild structure within the rollers studied was corroborated by the results obtained from the null model analysis (pseudo-assemblages). In all cases, very precise characterisation of the thermal niche was crucial to explaining the few instances of niche overlap observed. There was no evidence of interspecific competition in the roller assemblage that were studied. The only pairs of Canthon species that showed a significant, high degree of thermal niche overlap were C. femoralis and C. cyanellus cyanellus. Both species occupy similar thermal niches and have similar daily activity patterns ( Figs 2 and 3 ), but have different feeding habits. Canthon femoralis is a strict coprophage with a

preference for monkey excrement ( Castellanos et al. , 1999; Halffter, 2003 ) while C. cyanellus cyanellus is a strict necro-phage (with a certain tendency to necro-coprophagy in some locations) ( Halffter & Matthews, 1966 ). Similarly, D. lobipes and D. scabriusculum , two nocturnal species, avoid competition in spite of their affinity for the forest and even though they had the greatest overlap in thermal niche that was observed between sympatric species. In this case D. lobipes is a necrophagous spe-cies while D. scabriusculum is coprophagous ( Howden, 1966; Halffter, 2003 ).

Thus, as presented in the initial hypotheses, where there is sympatry with similar trophic habits, the species involved have very different thermal niches, and where there is a significant overlap in thermal niche between sympatric species, the trophic habits of the species are very different. The importance of T b on the spatial and temporal segregation of sympatric groups of spe-cies has been documented for diverse organisms. Pianka (1969) found a close relationship between the environmental subdivi-sion of habitat and resources in a community of lizards (based on T b ), emphasising that at least three dimensions were deter-mining the niche partitioning in several species of the genus Ctenotus : place, food, and time. Thermoregulation is likely to be one of the determining factors in habitat selection. However,

Fig. 2. The frequency distribution of fl ight for eight ball-rolling dung beetles distributed along an altitudinal gradient in central Veracruz, Mexico over a range of T a s.



it is not known how species use their thermoregulatory capacity or how species behave according to the thermal quality of the habitat, particularly in the case of the endothermic insects.

Ectothermic animals such as black rat snakes [ Elaphe obso-leta obsoleta (Say)] and some lacertid lizards [ Lacerta oxyc-ephala Duméril & Bibron, 1839 and Podarcis melisellensis (Braun, 1877)] have been observed to change thermoregulation pattern according to the thermal quality of the habitat ( Blouin-Demers & Weatherhead, 2002; Scheers & Van Damme, 2002 ). Thermoregulatory behaviour in amphibians is strongly affected by the physical nature of high tropical elevations and this ex-plains why only a few species have been able to exploit these extreme environments ( Navas, 1996 ). In ectothermic insects, specifically in grasshoppers, comparisons between two popula-tions of Circotettix rabula (Rehn & Hebard, 1906) revealed a great repertoire of thermoregulatory behaviour as a function of

thermal limitations imposed by altitudinal gradients ( Gillis & Smeigh, 1987 ).

In endotherms, results show limited thermoregulation pat-terns in this group as indicated by the boundaries of the thermal niches ( Fig. 3 ) and the normal distribution of flight tempera-tures in each one of the species of ball-rolling dung beetles studied ( Fig. 2 ). One aspect that helps to explain this is the pos-sibility that rollers may not coexist well with one another be-cause of their biology, and because of frequent and severe competition ( Hanski & Cambefort, 1991 ).

It is interesting that along the altitudinal gradient studied there are no Canthon species between 1000 and 1600 m a.s.l. Across this altitudinal band the only roller observed was D. mexicanum , a predominantly necrophagous species that is only found in the forest. This species is not very abundant in lower mountain forests and preferentially inhabits evergreen – oak forest between

Fig. 3. The relationship between T a and T ex for eight ball-rolling dung beetles distributed along an altitudinal gradient in central Vera-cruz, Mexico. For each species, the thermal niche was calculated by means of the ellipse formed by the standard deviation of the envi-ronmental temperature during fl ight (radius x ) and the standard deviation of the endother-mic capacity (radius y ). Abbreviations: cya, Canthon cyanellus ; fem, C. femoralis ; hum, C. humectus ; ind, C. indigaceus ; lob, Delto-chilum lobipes ; mex, D. mexicanum ; pse, D. pseudoparile ; sca, D. scabriusculum .

Table 2. Observed and expected mean and variance in the Czekanowski index for niche overlap measured on the ambient temperature recorded during fl ight. Number of pseudo-assemblages randomised 1000 times. See text for description of algorithms .

Mean niche overlap Niche overlap variance

Algorithm Observed Expected Tail probability Observed Expected Tail probability

RA 2 0.22 0.24 0.119 * 0.07 0.05 0.035 † RA 3 0.22 0.19 0.181 † 0.07 0.02 0.000 † RA 4 0.22 0.22 0.289 * 0.07 0.05 0.021 †

* Lower tail probability. † Upper tail probability.



1600 and 1800 m a.s.l. Why are small ball-roller species so scarce in forests at intermediate elevations? The results suggest that temperature is the most important factor affecting the pres-ence of these beetles. Tropical ball-rolling dung beetles need a minimum T a in order to be active (22.3 – 26.0 °C), so the rela-tively low temperatures of lower montane forests (mean annual temperature = 18.0 °C, minimum monthly temperature = 14.9 °C, maximum monthly temperature = 20.4 °C) reduce the colo-nisation possibilities for small roller species (with tropical af-finities) into these forests (J. R. Verdú, L. Arellano, C. Numa and E. Micó , unpublished data). For small roller beetles, thoracic warm up is particularly costly in energetic terms ( Caveney et al. , 1995 ), and apparently the relative low temperature of lower montane forests does not favour this activity for them.

Although thermal preference is usually roughly correlated with habitat ( May, 1979 ), at intermediate altitudes there are no coprophagous roller species common to open zones ( Canthon species), even though the pastures at these altitudes offer an abundance of cow dung. In comparison, the coastal plains have five species ( Halffter et al. , 1995 ) and in the mountain land-scape there is one species, C. humectus , a coprophage that for biogeographical reasons, a priori , and for thermoregulatory rea-sons, shown by the results of the present study, is not found in the intermediate and coastal landscapes. Canthon humectus (for which extreme values in the T a range and the highest T ex for a Canthonina species were recorded) belongs to an old lineage of tropical origin that evolved in and is adapted to the Mexican High Plateau. As such, this species is quite distinct from the lineages of Nearctic or Paleoamerican mountain origin that in Mexico comprise the true mountain fauna (see Halffter, 1987 ). On the altitudinal gradient studied, there is no proper upper oro-graphic limit such as a mountain peak (excluding the Cofre de Perote). Consequently, several species that are typical of the Plateau come down via the upper part of the gradient. Canthon humectus is distributed throughout the Plateau, even quite far to the north, and can come down the slopes.

The results of this study of the ball-rolling dung beetles along an altitudinal gradient support the concept of the thermal niche being a species-specific physiological constraint that can ex-plain the real and potential distribution of the species. Moreover, this concept can be used as a tool to explain the interspecific interactions of these species. Future research should be directed towards the search for and verification of the variables related to flight (minimum takeoff temperature, heat and cold shock tem-

peratures, thermal niche breadth, etc.) that could be influencing and predicting the geographic distribution of species in order to address such phenomena as vicariance and sympatry.

Acknowledgements

We thank E. Galante (CIBIO, Universidad de Alicante), J. M. Lobo (CSIC, Museo Nacional de Ciencias Naturales), and G. Halffter (Instituto de Ecología, A. C. Xalapa) for their observa-tions and recommendations throughout this study. Thanks also to B. Delfosse for improving the English of the manuscript and for her helpful comments. This research was supported by CONABIO-México (grants BE012, EE005), CONACYT (grant 37514-V), and AECI (A/1870/04 and A/3415/05).

References

Acosta , P.R . ( 1986 ) La vegetación de la Sierra de Manuel Díaz, Veracruz, México . BSc thesis , Facultad de Biología, Universidad Veracruzana , Veracruz, Mexico .

Albrecht , M. & Gotelli , N.J . ( 2001 ) Spatial and temporal niche parti-tioning in grassland ants . Oecologia , 126 , 134 – 141 .

Arellano , L . ( 1992 ) Distribución y abundancia de Scarabaeidae y Sil-phidae (Insecta Coleoptera) en un transecto altitudinal en el estado de Veracruz . Unpublished BSc thesis , Facultad de Ciencias . UNAM , México, Mexico .

Bartholomew , G.A. & Heinrich , B . ( 1978 ) Endothermy in African dung beetles during fl ight, ball making, and ball rolling . Journal of Experimental Biology , 73 , 65 – 83 .

Bestelmeyer , B . ( 2000 ) The trade-off between thermal tolerance and behavioural dominance in a subtropical South American ant com-munity . Journal of Animal Ecology , 69 , 998 – 1009 .

Blouin-Demers , G. & Weatherhead , P.J . ( 2002 ) Habitat-specifi c behav-ioural thermoregulation by black rat snakes ( Elaphe obsoleta obso-leta ) . Oikos , 97 , 59 – 68 .

Castellanos , M.C. , Escoba , R.F. & Stevenson , P.R . ( 1999 ) Dung beetles attracted to woolly monkey ( Lagothrix lagothrica Humboldt) dung at Tinigua National Park, Colombia . The Coleopterist’s Bulletin , 53 , 155 – 159 .

Castillo-Campos , G . ( 1985 ) Integración de paisajes en la región de Jalcomulco, Veracruz . Unpublished Bachelor thesis , Facultad de Bi-ología, Universidad Veracruzana, Veracruz , Mexico .

Castillo-Campos , G . ( 1991 ) Vegetación y Flora del Municipio de Xala-pa . Instituto de Ecología, A.C. y Ayuntamiento de Xalapa , Veracruz , Mexico .

Fig. 4. Cluster analysis of ball-rolling dung beetles distributed along an altitudinal gradi-ent in central Veracruz, Mexico. Dashed lines show species found in the intermediate land-scape ( Deltochilum mexicanum ) and from the high plateau landscape ( Canthon humectus ). Solid lines represent sympatric species found on the tropical coastal plains.



Caveney , S. , Scholtz , C.H. & McIntyre , P . ( 1995 ) Patterns of daily fl ight activity in onitine dung beetles (Scarabaeinae: Onitini) . Oecologia , 103 , 444 – 452 .

Cházaro-Basáñez , M.J . ( 1992 ) Exploraciones botánicas en Veracruz y estados circunvecinos. I. Pisos altitudinales de vegetación en el centro de Veracruz y zonas limítrofes con Puebla . La Ciencia y el Hombre , 10 , 67 – 115 .

Corbet , P.S . ( 1963 ) A Biology of Dragonfl ies . Quadrangle, Chicago , Illinois .

Díaz , A . ( 1998 ) Ecología y comportamiento de escarabajos rodadores del estiércol (Scarabaeidae: Scarabaeinae) de selvas y pastizales en Los Tuxtlas, Veracruz . Unpulished BSc thesis , Universidad Nacional Autónoma de México , Facultad de Ciencias, Maestría en Ecología y Ciencias Ambientales .

Feinsinger , P. , Spears , E.E. & Poole , R.W . ( 1981 ) A simple measure of niche breadth . Ecology , 62 , 27 – 32 .

Fincher , G.T. , Davis , R. & Bonner-Stewart , T . ( 1971 ) Flight activity of coprophagous beetles on a swine pasture . Annals of the Entomologi-cal Society of America , 64 , 855 – 860 .

Gillis , J.E. & Smeigh , P.A . ( 1987 ) Altitudinal variation in thermal be-havior of the grasshopper Circotettix rabula (Rehn and Hebard) from central Colorado . The Southwestern Naturalist , 32 , 203 – 211 .

Gotelli , N.J. & Entsminger , G.L . ( 2003 ) EcoSim: Null Models Software for Ecology , Version 7 . Acquired Intelligence Inc. and Kesey-Bear, Burlington , Vermont [WWW document]. URL http://homepages.together.net/~gentsmin/ecosim.htm [ accessed on 6 September 2004 ].

Halffter , G . ( 1987 ) Biogeography of the montane entomofauna of Mexico and Central America . Annual Review of Entomology , 32 , 95 – 114 .

Halffter , G . ( 2003 ) Tribu Scarabaeini . Atlas de los Escarabajos de Méxi-co, Coleoptera: Lamellicornia, Vol . II. Familias Scarabaeidae, Trogidae, Passalidae y Lucanidae ( ed . by M. A. Morón ), pp. 21 – 47 , Argania Editio , Barcelona .

Halffter , G. & Arellano , L . ( 2001 ) Variación de la diversidad en especies de Scarabaeinae como respuesta a la antropización de un paisaje tropical . Tópicos sobre Coleoptera de México ( ed . by J. L. Navarrete-Heredia , H. E. Fierros-López and A. Burgos-Solorio ), pp . 35 – 54 . Universidad de Guadalajara – Universidad Autónoma del Estado de Morelos , Guadajara, Mexico .

Halffter , G. & Arellano , L . ( 2002 ) Response of dung beetle diversity to human-induced changes in a tropical landscape . Biotropica , 34 , 144 – 154 .

Halffter , G. & Edmonds , W.D . ( 1982 ) Evolución de la nidifi cación y de la cooperación bisexual en Scarabaeinae (Ins.: Col .). Anales de la Escuela Nacional de Ciencias biológicas de México , 25 , 117 – 144 .

Halffter , G. , Favila , M.E. & Arellano , L . ( 1995 ) Spatial distribution of three groups of Coleoptera along an altitudinal transect in the Mexi-can transition zone and its biogeographical implications . Elytron , 9 , 151 – 185 .

Halffter , G. & Matthews , E.G . ( 1966 ) The natural history of dung bee-tles of the subfamily Scarabaeinae . Folia Entomológica Mexicana , 12 – 14 , 1 – 312 .

Hamilton , W.J . ( 1975 ) Coloration and its thermal consequences for diur-nal desert insects . Environmental Physiology of Desert Organisms ( ed . by N. F. Hadley) , pp. 67 – 89. Halsted , Stroudsburg, Pennsylvania .

Hanski , I. & Cambefort , Y . ( 1991 ) Competition in dung beetles . Dung Beetle Ecology ( ed . by I. Hanski and Y. Cambefort ), pp . 305 – 329 . Princeton University Press , Princeton, New Jersey .

Heinrich , B . ( 1993 ) Hot-blooded Insects: Strategies and Mecha-nisms of Thermoregulation . Harvard University Press , Cambridge, Massachusetts .

Heinrich , B. & Bartholomew , G.A . ( 1979 ) Roles of endothermy and size in inter- and intraspecifi c competition for elephant dung in an African dung beetle, Scarabaeus laevistriatus . Physiological Zoology , 52 , 484 – 496 .

Holm , E. & Edney , E.B . ( 1973 ) Daily activity of Namib Desert arthro-pods in relation to climate . Ecology , 54 , 45 – 56 .

Howden , H.F . ( 1966 ) Notes on Canthonini of the “Biologia Centrali-Americana” and descriptions of new species (Coleoptera, Scarabaei-dae) . The Canadian Entomologist , 98 , 725 – 741 .

May , M.L . ( 1979 ) Insect thermoregulation . Annual Review of Entomology , 24 , 313 – 349 .

May , M.L . ( 1985 ) Thermoregulation . Comprehensive Insect Physiology Biochemistry and Pharmacology ( ed . by G. A. Kerkut and L. I. Gilbert ), pp . 507 – 552 . Pergamon, Oxford .

Mena , J. , Galante , E. & Lumbreras , C.J . ( 1989 ) Daily fl ight activity of Scarabaeidae and Geotrupidae (Col.) and analysis of the factors determining this activity . Ecologia Mediterranea , 15 , 69 – 80 .

Narave , F.H . ( 1985 ) La vegetación del Cofre de Perote, Veracruz, México . Biótica , 10 , 35 – 63 .

Navas , C.A . ( 1996 ) Implications of microhabitat selection and patterns of activity on the thermal ecology of high elevation neotropical anurans . Oecologia , 108 , 617 – 626 .

Pereboom , J.J.M. & Biesmeijer , J.C . ( 2003 ) Thermal constraints for stingless bee foragers: the importance of body size and coloration . Oecologia , 137 , 42 – 50 .

Pianka , E.R . ( 1969 ) Sympatry of desert lizards ( Ctenotus ) in western Australia . Ecology , 50 , 1012 – 1030 .

Robles , H.L . ( 1986 ) La vegetación y uso tradicional de las plantas de la Barranca de Monterrey, Municipio de Axoxuapan, Ver., y sus alred-edores . Unpublished BSc thesis , Facultad de Biología, Universidad Veracruzana, Veracruz , Mexico .

Scheers , H. & Van Damme , R . ( 2002 ) Micro-scale differences in ther-mal habitat quality and a possible case of evolutionary fl exibility in the thermal physiology of lacertid lizards . Oecologia , 132 , 323 – 331 .

Schoener , T.W . ( 1974 ) Resource partitioning in ecological communi-ties . Science , 185 , 27 – 39 .

StatSoft Inc . ( 1997 ) STATISTICA for Windows ( Computer program manual ). Tulsa , Oklahoma .

Verdú , J.R. , Arellano , L. & Numa , C . ( 2006 ) Thermoregulation in endo-thermic dung beetles (Coleoptera: Scarabaeidae): effect of body size and ecophysiological constraints in fl ight . Journal of Insect Physiology , 52 , 854 – 860 .

Verdú , J.R. , Díaz , A. & Galante , E . ( 2004 ) Thermoregulatory strategies in two closely related sympatric Scarabaeus species (Coleoptera: Scarabaeinae) . Physiological Entomology , 29 , 32 – 38 .

Winemiller , K.O. & Pianka , E.R . ( 1990 ) Organization in natural assem-blages of desert lizards and tropical fi shes . Ecological Monographs , 60 , 27 – 55 .

Ybarrondo , B.A. & Heinrich , B . ( 1996 ) Thermoregulation and response to competition in the African dung beetle Kheper nigroaeneus (Cole-optera: Scarabaeidae) . Physiological Zoology , 69 , 35 – 48 .

Zamora , P . ( 1992 ) Flora vascular del municipio de San Andrés Tlalne-huayocan . Unpublished BSc thesis , Facultad de Biología, Universi-dad Veracruzana, Veracruz , Mexico .

Accepted 5 April 2007

Roles of endothermy in niche differentiation for ball-rolling dung beetles (Coleoptera:...

Documents

Transcript of Roles of endothermy in niche differentiation for ball-rolling dung beetles (Coleoptera:...