High diversity beetle assemblages attracted to carrion and dung in threatened tropical oak forests in Southern Mexico

ORIGINAL PAPER

High diversity beetle assemblages attracted to carrion and dungin threatened tropical oak forests in Southern Mexico

Ubaldo Caballero • Jorge L. Leon-Cortes

Received: 23 March 2011 / Accepted: 19 September 2011 / Published online: 30 September 2011

� Springer Science+Business Media B.V. 2011

Abstract Despite high diversity levels of beetles inhab-

iting dung and carcasses, very few studies have attempted a

comparative assessment of copro-necrophile beetle com-

munities in relation to spatio-temporal variations, particu-

larly in the tropics where the vast majority of beetles occur.

We compared beetle assemblages attracted to pads of cattle

dung and rat carcasses in four contrasting vegetation types

associated with oak forest. In a total of 52 transects

including 3,952 dung pad days and 2,600 carcass-trap days

we recorded 14,989 beetles representing 406 species and

33 families. Necrophiles (323 species and 33 families)

were considerably more diverse than coprophiles (172

species and 16 families). Staphylinidae were taxonomically

and numerically dominant, comprising 45% of species and

66% of individuals, respectively. Species estimators (Chao

2) suggested that the observed beetle richness represented

68% of coprophile and 56% of necrophile species richness,

with rare species constituting the majority of the species:

singletons and doubletons = 89 species (52%) of copro-

philes and 166 species (51%) of necrophiles. Beetle

assemblages varied in diversity and composition as regards

to vegetation type and season: samples from less disturbed

vegetation types (continuous oak forest and ravines) had

higher beetle diversity, and a strong seasonality effect was

recorded for necrophiles, but not for coprophiles. In addi-

tion, an indicator value analysis (IndVal), showed that

relatively preserved vegetation types recorded more indi-

cator species as compared to disturbed sites. Our studies

clearly demonstrates that the least fragmented oak forest

and ravine are the most valuable areas for necrophile and

coprophile beetles in Neotropical Mexico, especially for

specialist beetles.

Keywords Carrion � Chiapas � Coleoptera � Community

ecology � Dung � Neotropical region

Introduction

Dung pads and carcasses represent discrete, ephemeral,

patchy resources of highly concentrated energy which are

widespread throughout a variety of habitats, and to which

many insect species are adapted (Hanski 1983; Putman

1983; Doube 1987; Shorrocks 1990). By taking part in the

decomposition processes, insects promote persistence of

local plants and a variety of trophic interactions (including

bacteria, fungi, protozoa, nematodes; Carter et al. 2007;

Parmenter and MacMahon 2009). Insects, especially

Coleoptera, are one of the most diverse components of

dung and carrion substrates, with over 100 and 200 beetle

species recorded on single cattle dung pads and carcasses,

respectively (Payne 1965; Bernon 1981).

An important implication of the spatio-temporal patch-

iness of carrion and dung relates to the tight dependency of

their insect faunas, rendering them highly sensitive to

habitat loss and fragmentation (Klein 1989; Trumbo and

Bloch 2000; Halffter and Arellano 2002). This is particu-

larly true in tropical regions, where large areas of forest

have been converted into complex landscape mosaics

dominated by secondary forest fragments and agro-pastoral

systems (Dirzo and Raven 2003; Lamb et al. 2005). Many

other taxonomic groups have been negatively influenced by

these effects (Fahring 2003).

U. Caballero � J. L. Leon-Cortes (&)

Departamento de Ecologıa y Sistematica Terrestre, El Colegio

de la Frontera Sur, Carr. Panamericana y Av. Periferico Sur S/N,

San Cristobal de las Casas, Chiapas 29290, Mexico

e-mail: [email protected]

123

J Insect Conserv (2012) 16:537–547

DOI 10.1007/s10841-011-9439-y

Previous surveys have assessed the impacts of distur-

bance and habitat fragmentation upon complex and diverse

copro-necrophile beetle communities (Davis 1994; Dunn

and Danoff-Burg 2007; Ulrich et al. 2008). Sometimes

studies narrowly focus on Scarabaeinae dung beetle

assessments (see Nichols et al. 2007), whereas only a

limited number of surveys have considered the assessment

of others key groups such as carrion beetles (Silphidae; e.

g. Gibbs and Stanton 2001; Trumbo and Bloch 2000; Wolf

and Gibbs 2004; Creighton et al. 2009) and rove beetles

(Staphylinidae; e.g. Pohl et al. 2007; Caballero et al. 2009;

Vasquez-Velez et al. 2010). It would therefore be extre-

mely important to quantify comparative responses of the

copro-necrophile beetle communities particularly in Neo-

tropical systems, where, to our knowledge, no attempt has

been made to do so, and where a complete understanding

on the effects of habitat fragmentation and on the relative

importance of habitat type and conditions on complex

guilds are needed for effective management and conser-

vation. Both carrion and dung have been extensively used

to estimate and monitor beetle local populations safely

(Payne 1965; Putman 1983), and hence this procedure

allowed us to maximize insect collections along the whole

decomposition process (Holter 1982; Putman 1983).

We conducted a comparative detailed study of copro-

necrophile beetles in four vegetation types associated with

fragmented oak forests in southern Mexico. Our particular

aims were (i) to evaluate the relative effects of vegetation

type and seasonality on diversity and composition of

these two beetle communities in oak forest remnants, and

(ii) based on species association and diversity, to identify

the relative importance of particular vegetation types for

species conservation. A set of important predictions of

our assessment relates to significant negative changes in

species composition and abundance for sensitive groups

(i.e. Hydrophilidae, Leiodidae, Nitidulidae, Silphidae)

moderate or no changes for relatively generalist guilds

(i.e. Carabidae, Histeridae), and positive changes for

common and widely distributed groups (i.e. Scarabaei-

deae, Staphylinidae), in relation to vegetation small-scale

variations.

Materials and methods

Study area

Four vegetation types associated with oak forests were

studied in southern Mexico. Three of which were located in

the San Fernando Valley (16�4804800N, 93�1004200W): (1) a

highly fragmented oak forest, referred to as ‘‘fragmented

oak forest’’; (2) an area dominated by savannah vegetation

with scattered quarries referred as ‘‘savannah’’; (3) an area

at the bottom of a canyon that has seasonal streams and

interspersed with oak forest patches, referred as ‘‘ravines’’.

Because continuous, little-disturbed oak forests are

practically nonexistent in the San Fernando Valley, we

chose a forest in the highlands, approximately 55 km to the

east, as point of comparison. This non-fragmented tropical

oak forest is located in the Biological Reserve Cerro Hu-

itepec (16�4403800N, 92�4001500W), referred to as ‘‘contin-

uous oak forest’’ (for further details see Caballero et al.

2009). Mean annual temperature and rainfall are 26�C and

883 mm for San Fernando and 15�C and 1,200 mm for

Huitepec (CNA 2006). San Fernando is highly seasonal,

with the wet season concentrated from May to October, and

the dry season from November to April; 81% of the pre-

cipitation falls between June and September. In Huitepec,

rainfall does fluctuate seasonally, but its dry season

encompasses a very short period of the year (from

December to March; Anonymous 2006).

Sampling design

In each vegetation type, at least four 50-m linear transects

were established (one transect corresponding to one sam-

ple, and the number of transects per vegetation type during

both seasons as replicates, N = 52, Table 2). Along each

transect, we exposed fresh baits (rat carcasses and dung

cattle pads) to quantify beetle species and abundance

through time. In order to register the fauna during con-

trasting conditions of the year, we carried out field work

distributed in two sampling periods during dry (March–

early June) and wet seasons (August–October, 2005),

except for ‘‘continuous oak forest’’ sites where only sam-

ples during the rainy season were taken (May–July, 2006).

Coprophilous beetle sampling

Along each transect, a 1 kg pad of fresh cattle dung was

placed every 5 m, making a total of 10 dung pads per

transect. Every day we removed one pad from each transect

for the first 7 days and then after 10, 15 and 23 days

(N = 520 dung pads). Beetles were extracted by putting

each pad in water (ca 20 l); then collecting the beetles as

they floated to the surface (Moore 1954). All insects were

placed in 70% ethanol. Beetles which burrowed beneath

the dung were hand-collected.

Necrophilous beetle sampling

Recent killed laboratory rats (Rattus norvegicus L.) were

used as baits. A fresh rat carcass (weight 80–100 g) was

placed in a pitfall trap as described by Kocarek (2000). The

trap was placed in a wire mesh cylinder with 1.5 cm holes

in order to avoid disturbance by vertebrate scavengers.

538 J Insect Conserv (2012) 16:537–547

123

A fixing liquid of ethylene glycol–water in a 1:1 proportion

was added to a vessel below the carrion, and the cylinder

was buried at the soil surface (Kocarek 2000).

Along each transect, one trap was located (Total N = 52

traps) and inspected for insects daily for the first 7 days,

every other day from day 9 to 20th, and twice a week for

the rest of the sampling period. The total time of bait

exposure was 3,952 dung-pad days and 2,600 carcass-trap

days.

Beetles were identified to the family level using Borror

et al. (1989) and Arnett et al. (2002). All specimens were

sorted to morphospecies using the guidelines of Oliver and

Beattie (1996). In problematic specimens, genitalia were

dissected and sent to specialists for species identification

(see Acknowledgments). A reference series of each mor-

phospecies was deposited in the entomological collection

of El Colegio de la Frontera Sur (ECOSC-E), San Cristobal

de las Casas, Mexico. For simplicity, we hereafter refer to

morphospecies as species.

Data analysis

We compared sample-based rarefaction curves (at compa-

rable levels of sampling effort) by scaling the x-axis to the

number of transects (obtaining species density curves;

Gotelli and Colwell 2001). This method is particularly useful

if assemblages have been assessed under different sampling

intensity or success (Gotelli and Colwell 2001), as in our

case. We contrasted values for: (a) the total number of spe-

cies recorded for coprophiles and necrophiles, (b) the total

number of species recorded for coprophiles and necrophiles

between dry and rainy seasons, (c) the total number of spe-

cies recorded for coprophiles and necrophiles among four

vegetation types, and (d) the number of species recorded in

each vegetation type for coprophiles and necrophiles

between dry and rainy seasons.

To compare the diversity as stated above in (c) and (d),

we computed Fisher’s alpha, a widely-used diversity index

that is relatively unbiased to sampling intensity (Magurran

2004). In addition, species richness for dominant

beetle families was compared using Mann–Whitney U or

Kruskal–Wallis tests among vegetation types and between

dry and rainy seasons. For all tests, statistical significance

was taken after Bonferroni correction for multiple com-

parisons (Sokal and Rohlf 1995).

To estimate total species richness numbers for vegeta-

tion types we used Chao2, a non-parametric statistical

estimator to reduce potential bias due to potential incom-

plete sampling (Chao 2005).

We also calculated the number of ‘‘rare’’ species defined

as singletons and doubletons (i.e. those which recorded:

only one individual and only two individuals, respectively,

see Novotny and Basset 2000).

We examined the similarity for coprophiles and necro-

philes among vegetation types by computing an abun-

dance-based Sørensen index of similarity developed by

Chao et al. (2005), since this approach reduces the potential

bias of undersampling when differences are in sample size

(Chao et al. 2005). In addition, as sampling effort within

vegetation types was equivalent, seasonal similarity within

vegetation types was examined using Sørensen index

(Magurran 2004). All calculations were performed using

EstimateS 8.2.0 (Colwell 2009).

We calculated a measure of dominance using the pro-

portion of individuals for the commonest species in a given

vegetation type (Berger-Parker index) (Magurran 2004).

Dominance values (for coprophiles and necrophiles) were

estimated for dry and rainy seasons and for each vegetation

type in each season. In addition, to elucidate dominance

patterns within local communities, we plotted species-

abundance distributions for coprophiles and necrophiles

(Whittaker plots) recorded in each vegetation type. By

regressing species rank and species abundance (Magurran

2004), we examined potential deviations of the slopes of

the linear equations as regards to vegetation type—the

lower the value of the slope of each regression line the

greater the evenness of the assemblage (Tokeshi 1993). All

statistical analyses were performed using SPSS 15�.

Species-vegetation associations were identified based on

the indicator value method (IndVal, see Dufrene and

Legendre 1997). IndVal analysis allowed us to identify

indicator species within each vegetation type. All species

that recorded at least 10 individuals in samples were con-

sidered for analysis.

Results

Beetle fauna

We collected a total of 14,989 beetles representing 406

species and 33 families, of which 5,255 individuals, 172

species and 16 families were recorded in dung pads, and

9,734 individuals, 323 species and 33 families in rat car-

casses (Table 1). Family richness among vegetation types

ranged from 7 to 9 families for coprophiles and from 14 to

21 for necrophiles (Table 2). Staphylinidae was the most

diverse family, followed by Scarabaeidae and Histeridae

(Table 1). Staphylinids were represented by 83 species of

coprophiles and 142 species of necrophiles, including 73

and 63% of the total abundance, respectively (Table 1).

Rare species constituted the majority of the species: sin-

gletons and doubletons = 89 species (52%) of coprophiles

and 166 species (51%) of necrophiles (Table 2). However,

for coprophiles, the singletons’ curve appeared to reach an

asymptotic behavior (Fig. 1a). The 20 commonest species

J Insect Conserv (2012) 16:537–547 539

123

in each substrate accounted for 81 and 73% of the total

number of individuals of coprophiles and necrophiles,

respectively. Two species of staphylinids, namely Platy-

stethus sp. for coprophiles, and Hoplandria sp. for necro-

philes, represented the dominant species and accounted for

the 34 and 12% of the total number of individuals.

The estimated total number of species indicated a

reasonable level of completeness (Chao2 = 68% for

coprophiles and 56% for necrophiles). Among vegetation

types, coprophiles recorded higher values of complete-

ness (57–79%) than necrophiles (31–71%), and ravines

recorded the lowest total richness values (57% for copro-

philes and 31% for necrophiles; Table 2).

Species density and diversity patterns

Rarefaction curves showed necrophiles as relatively more

diverse than coprophiles (Fig. 1a). Among vegetation

types, continuous oak forest recorded the highest beetle

density for necrophiles, although for coprophiles no

differences were detected. However, ravines showed a

markedly steeper slope relative to other vegetation types

Table 1 Beetles species assemblages of coprophiles (Copr) and necrophiles (Necr) recorded in four contrasting vegetation types in Chiapas,

Southern Mexico

Family Species richness Abundance % Total abundance

Copr Necr Copr Necr Copr Necr

Anthicidae 5 1 10 10 0.19 0.1

Archeocrypticidae 0 2 0 26 0 0.27

Bostrichidae 0 2 0 3 0 0.03

Carabidae 6 15 55 110 1.05 1.13

Cleridae 0 2 0 5 0 0.05

Colydiidae 1 1 1 1 0.02 0.01

Cryptophagidae 2 5 2 89 0.04 0.91

Curculionidae 0 8 0 16 0 0.16

Dermestidae 0 2 0 2 0 0.02

Elateridae 0 2 0 5 0 0.05

Histeridae 17 19 427 792 8.13 8.14

Hydrophilidae 9 21 120 204 2.28 2.10

Laemophloeidae 1 1 1 1 0.02 0.01

Leiodidae 0 13 0 771 0 7.92

Limnichidae 0 2 0 9 0 0.09

Melyridae 1 1 1 1 0.02 0.01

Monommatidae 0 4 0 12 0 0.12

Monotomidae 0 1 0 2 0 0.02

Mycetophagidae 0 2 0 4 0 0.04

Nitidulidae 7 27 17 769 0.32 7.90

Nosodendridae 1 1 11 1 0.21 0.01

Phalacridae 0 4 0 4 0 0.04

Ptiliidae 1 2 1 67 0.02 0.69

Ptilodactylidae 2 2 13 5 0.25 0.05

Salpingidae 0 1 0 1 0 0.01

Scarabaeidae 32 26 738 601 14.04 6.17

Scydmaenidae 0 3 0 28 0 0.29

Silphidae 0 1 0 9 0 0.09

Silvanidae 0 1 0 1 0 0.01

Staphylinidae 83 142 3,849 6,108 73.24 62.75

Tenebrionidae 3 6 7 44 0.13 0.45

Trogidae 0 2 0 30 0 0.31

Trogossitidae 1 1 2 3 0.04 0.03

TOTAL 172 323 5,255 9,734 100 100

540 J Insect Conserv (2012) 16:537–547

123

(at comparable levels of sampling effort, Fig. 1c, d), and

Fisher’s alpha values among vegetation types were con-

sistent with this finding (see Fig. 1c, d; Table 2). Species

richness for coprophile-Scarabaeidae (Kruskal–Wallis:

v2p0.008, 3 = 16.29, P = 0.001) and for necrophile-Nitidu-

lidae and Scarabaeidae (Kruskal–Wallis: v2p0.008, 3 =

20.52, P \ 0.000; v2p0.008, 3 = 12.39, P = 0.006; respec-

tively) varied significantly among vegetation types. We

identified statistically significant differences for the values

of species richness for coprophile-Hydrophilidae (Mann–

Whitney U = 106, P \ 0.008, N = 24) and Scarabaeidae

(Mann–Whitney U = 142.5, P \ 0.002, N = 24) between

dry and rainy seasons; and for necrophile-Leiodidae

(Mann–Whitney U = 108, P \ 0.008, N = 24), Nitiduli-

dae (Mann–Whitney U = 32, P \ 0.008, N = 24), Scara-

baeidae (Mann–Whitney U = 73.5, P \ 0.000, N = 24),

and Staphylinidae (Mann–Whitney U = 6.5, P \ 0.008,

N = 24), between dry and rainy seasons.

On the other hand, abundance rank distributions differed

among vegetation types: ravines and fragmented oak forest

(for coprophiles), and continuous oak forest and frag-

mented oak forest (for necrophiles) included more even

beetle communities (Fig. 2).

Beetle similarity among vegetation types

Chao-Sørensen estimates indicate that continuous oak

forests were the least similar community compared to

communities of other habitats, which were all relatively

similar. Other pair-wise vegetation type comparisons

showed relatively similar beetle communities (Table 3).

Effects of seasonality

Species density for necrophiles differed significantly

between seasons, but not for coprophiles (Fig. 1b). How-

ever, coprophiles were more diverse during the dry season

and necrophiles during the rainy season (Fisher’s alpha dry

vs. rainy season (SD) = 18.7 (0.9) vs. 15.9 (0.8) for co-

prophiles and 16.1 (0.9) vs. 26.7 (1) for necrophiles).

Ravines recorded the highest diversity for beetles in both

substrates during the dry season (Fig. 1e, g), although

during the rainy season, beetle diversity was similar among

vegetation types (Fig. 1f, h). A marked dissimilarity in the

faunal composition between the dry and wet period was

recorded for all vegetation types examined (Table 2).

Figure 3 shows the proportions of the number of indi-

viduals and species per family among vegetation types

during dry and rainy seasons. Staphylinidae was dispro-

portionately dominant in most vegetation types. Continu-

ous oak forests recorded the highest number of families and

an evenly distribution of the proportions for necrophilesTa

ble

2S

um

mar

yst

atis

tics

for

each

veg

etat

ion

typ

est

ud

ied

Veg

etat

ion

typ

eT

ran

sect

sp

er

veg

etat

ion

typ

e

No

.in

div

idu

als

No

.sp

ecie

sN

o.

fam

ilie

sN

o.

sin

gle

ton

s�(%

)*F

ish

er’

alp

ha

(±S

D)

Ch

ao2

§(%

)S

øre

nse

n�

Co

pr

Nec

rC

op

rN

ecr

Co

pr

Nec

rC

op

rN

ecr

Co

pr

Nec

rC

op

rN

ecr

Co

pr

Nec

r

Co

nti

nu

ou

so

akfo

rest

46

70

4,1

51

45

15

39

20

21

(47

)5

8(3

8)

11

.2(1

.5)

31

.3(1

.2)

73

(62

)2

48

(62

)–

–

Fra

gm

ente

do

akfo

rest

12

1,4

90

2,7

74

85

12

47

21

24

(28

)5

9(4

8)

13

.2(2

)1

3.1

(1.2

)1

08

(79

)3

17

(39

)0

.48

0.2

5

Rav

ine

85

22

2,1

31

73

72

81

43

2(4

4)

35

(49

)1

9(0

.7)

11

(0.8

)1

63

(57

)2

32

(31

)0

.24

0.3

6

Sav

ann

ah4

2,5

73

67

86

47

78

17

24

(37

)3

1(4

0)

8.1

(0.9

)1

3.2

(0.7

)1

05

(67

)1

08

(71

)0

.39

0.1

2

To

tal

28

5,2

55

9,7

34

17

23

23

16

33

61

(35

)1

32

(41

)3

4.4

(1.2

)6

4(1

.6)

25

2(6

8)

58

0(5

6)

0.4

10

.35

Ch

ao2

isn

on

par

amet

ric

esti

mat

or

of

tota

lsp

ecie

sri

chn

ess,

incl

ud

ing

un

det

ecte

dsp

ecie

s

Co

pr

Co

pro

ph

iles

,N

ecr

Nec

rop

hil

es,

DS

Dry

seas

on

,R

SR

ain

yse

aso

n�

Nu

mb

ero

fsp

ecie

sre

pre

sen

ted

by

on

esp

ecim

en

(%)*

Per

cen

tag

eo

fth

eto

tal

catc

hfo

rea

chv

eget

atio

nty

pe

§P

erce

nta

ge

of

Ch

ao2

esti

mat

edsp

ecie

sth

atw

ere

reco

rded

on

each

veg

etat

ion

typ

e�

Sim

ilar

ity

abu

nd

ance

bas

ed(S

øre

nse

nin

dex

)b

etw

een

dry

and

rain

yse

aso

ns

for

the

tota

lfa

un

aan

dfo

rea

chv

eget

atio

nty

pe

inS

anF

ern

and

o

J Insect Conserv (2012) 16:537–547 541

123

but not for coprophiles (Fig. 3). Dominance was higher in

the dry season for both substrates (Berger–Parker: dry

season, d = 0.55; rainy season, d = 0.23 for coprophiles

and dry season, d = 0.4; rainy season, d = 0.19 for

necrophiles).

Finally, an IndVal analysis detected indicator species for

all vegetations types (35 species of coprophiles and 58

species of necrophiles, P \ 0.05 and IndVal value C 25).

Relatively preserved vegetation types (continuous oak

forest and ravine) recorded more indicator species in

relation with disturbed sites (fragmented oak forest and

savannah, see Tables 4, 5).

Discussion

Despite high diversity levels of beetles inhabiting dung and

carcasses, this is, to our knowledge, the first study that

attempted a comparative survey of copro-necrophile beetle

communities in relation to vegetation spatio-temporal

variations in Mexico. Our results in four contrasting veg-

etation types associated to oak forests showed an amassing

0

20

40

60

80

100

120Necrophiles dry season

S

RFOF

Number of transects

0

20

40

60

80

100Total by vegetation type (Cop)

S

FOF

R

COF

0

20

40

60

80Coprophiles rainy season

R

FOF

S

0

30

60

90

120Necrophiles rainy season

R

FOF

S

0

50

100

150

200Total by vegetation type (Nec)

S

COF FOF

R

0

20

40

60

80 Coprophiles dry season

S

R

FOF

0

50

100

150

200

250

300

350Necrophiles

Coprophiles

Singletons Cop

Singletons Nec

Nu

mb

er o

f sp

ecie

s

0

50

100

150 Total by season

Nec DS

Nec RS

Cop DSCop RS

(g)

S

RFOF

(c)

S

FOF

R

COF

(f)

R

FOF

S

0

30

60

90

120(h)

R

FOF

S

0

50

100

150

200(d)

S

COF FOF

R

(e)

S

R

FOF

(a) Necrophiles

Coprophiles

Singletons Cop

Singletons Nec

0 3 6 9 12 15

0 5 10 15 20 25

0 3 6 9 12 15 0 3 6 9 12 15

0 5 10 15 20 25

0 3 6 9 12 15

0 10 20 30 40 50 60 0 5 10 15 20 25 30

(b)

Nec DS

Nec RS

Cop DSCop RS

Total coleoptera

Fig. 1 Species density rarefaction curves with 95% confidence

intervals (dashed lines) for a total number of coprophiles, necrophiles

and singletons, b coprophiles and necrophiles collected during dry

and rainy season, c coprophiles and d necrophiles recorded in each

vegetation type, e, f coprophiles and g, h necrophiles in San Fernando

for dry and rainy seasons. Vertical lines indicate standardized sample

sizes. Cop Coprophiles, Nec Necrophiles, DS dry season, RS rainy

season, COF continuous oak forest, FOF fragmented oak forest,

R ravine, S savannah

0

0.5

1

1.5

2

2.5

3

3.5

Species rank

Coprophiles

Continuous oak forest (-0.043)

Fragmented oak forest (-0.025)

Ravine (-0.022)

Savannah (-0.038)

(a)

0

0.5

1

1.5

2

2.5

3

3.5

0 30 60 90 120 150

0 30 60 90 120 150

Species rank

Necrophiles

Continuous oak forest (-0.015)

Fragmented oak forest (-0.018)

Ravine (-0.03)

Savannah (-0.021)

(b)

Log 1

0(a

bund

ance

)

Fig. 2 Rank-abundance curves (Whittaker’s plots) of each vegetation

type studied. Numbers in parentheses are the slope values of linear

regression equations of rank values for the abundance (log10 ?1) of

each species

Table 3 The Chao-Sørensen similarity index values among pairs of

vegetation types

COF FOF Coprophiles

Savannah Ravine

COF – 0.28 0.33 0.12

FOF 0.02 – 0.96 0.84

Savannah 0.02 0.92 – 0.78

Ravine 0.02 0.91 0.72 –

Necrophiles

COF continuous oak forest, FOF fragmented oak forest

542 J Insect Conserv (2012) 16:537–547

123

beetle diversity including 14,989 beetles representing 406

species and 33 families. This recorded number of necro-

phile and coprophile beetles represents a 29% of the beetle

families reported for Mexico and 26% for the Neotropics

(Costa 2000; Navarrete–Heredia and Fierros–Lopez 2001).

Nonetheless, in our habitat surveys we detected dissimilar

0

20

40

60

80

100

FOF (DS)FOF (RS) Rav (DS) Rav (RS) Sav (DS) Sav (RS) COFN

o. s

peci

es (

%)

(d) 2011 8 9 101312†

0

20

40

60

80

100

FOF (DS)FOF (RS) Rav (DS) Rav (RS) Sav (DS) Sav (RS) COF

No.

indi

vidu

als

(%)

(a) 0.215* 0.333 0.181 0.817 0.3610.1290.409

0

20

40

60

80

100


No.

spe

cies

(%

)

(b) 1067 9 7 8 6†

Coprophiles

0

20

40

60

80

100


No.

indi

vidu

als

(%)

0.143* 0.491 0.4 0.793 0.2630.1430.778

Necrophiles

Stap Scar Hist Niti Car Leio Other BeetlesHydr Trog

(c)

Fig. 3 Family proportion of coprophiles and necrophiles beetles

collected in four vegetation types in dry and rainy seasons. The

category of ‘‘other beetles’’ comprises 25 families representing 10 and

18% of the species and 1 and 3% of the abundance of coprophiles and

necrophiles, respectively. COF continuous oak forest, FOF frag-

mented oak forest, R ravine, S savannah, DS dry season, RS rainy

season. *Dominance (Berger-Parker index), �No. families

Table 4 Coprophilous beetle indicator species of each vegetation type using the IndVal analysis

COF FOF Ravine Savannah

Hydrophilidae Staphylinidae Histeridae Carabidae

Cercyon sp. 6 (100)** Aleochara oxypodia (51)* Euspilotus sp.2 (50)** Apristus mexicanus (25)*

Scarabaeidae Histeridae sp. 2 (38)* Scarabaeidae

Aphodinae sp. 10 (100)** Scarabaeidae Euoniticellus intermedius (52)**

Onthophagus cyanellus (100)** Uroxys sp. 1 (73)** Aphodinae sp. 5 (45)**

Onthophagus sp. 1 (100)** Aphodinae sp. 3 (44)** Staphylinidae

Aphodinae sp. 2 (99)** Staphylinidae Platystethus sp. (80)**

Staphylinidae Coproporus hepaticus (86)** Aleochara notula (69)**

Anotylus sp. 3 (100)** Anotylus sp. 1 (75)** Tinotus sp. 1 (62)**

Atheta sp. 10 (100)** Lissohypnus sp. 1 (50)** Phylonthus sp.1 (45)*

Myllaena sp. (100)** Belonuchus rufipennis (48)*

Oxytelus sp. (100)** Lithocharis sp. (33)*

Tinotus caviceps (100)** Neohypnus sp.1 (32)*

Atheta sp. 9 (85)**

Indicator value is given in parenthesis. Significance of Monte Carlo test: *P \ 0.05; **P \ 0.01

Names in bold denote beetle families

J Insect Conserv (2012) 16:537–547 543

123

responses between beetle assemblages among vegetation

types that might be related to particular preferences of each

group as well as to inherent effects of seasonally and

vegetation type conditions.

First, an examination of the diversity for coprophile

beetle families revealed that Staphylinidae and Scarabaei-

deae showed no strong differences for vegetation type

preferences (although see below; Davis et al. 1988; Dunn

and Danoff-Burg 2007; Caballero et al. 2009; Hopp et al.

2010). Staphylinidae are generalist predators (Hanski

1987), and most dung beetles—Scarabaeideae- are con-

sidered opportunistic—they tend to use a large variety of

dung types (Hanski and Cambefort 1991). The Histeridae

were relatively common and widely distributed across

vegetation types—except in continuous oak forests where

they were absent, likely because the margins of Histeridae

populations might be affected by physiographic habitat

boundaries—previous findings have shown a negative

effect of elevation on their distributions (Kovarik and

Caterino 2001). The Hydrophilidae, which are consumers

of dung (Didham et al. 1998), were more abundantly

trapped in ravines and continuous oak forests. Intriguingly,

the Nitidulidae, although mostly saprophagous and myce-

tophagous, were observed in the ravine during the rainy

season (in San Fernando), most likely reflecting their

opportunist foraging habits: they have been observed

feeding on a widely decaying substrates (Didham et al.

1998).

On the other hand, necrophile beetles exhibited con-

trasting patterns. The Staphylinidae, Scarabaeideae, and

Histeridae families were evenly distributed across vegeta-

tion types (except by the absence of Histeridae in contin-

uous oak forests), and showing a clear decrease in

abundance in the Savannah. The Hydrophilidae showed

relatively constant abundances across vegetation types,

except in the Savannah where they were absent. The Lei-

odidae are mostly scavengers that feed on various decaying

organic materials in usually moist forest (Peck 2001),

which might explain their presence in ‘‘forested’’ condi-

tions during the rainy season (oak forests and ravines).

Interestingly, the Carabidae were almost exclusively

present during the dry season in fragmented oak forests,

Table 5 Necrophilous beetle indicator species of each vegetation type using the IndVal analysis

COF FOF Ravine Savannah

Carabidae Staphylinidae Scarabaeidae Histeridae Staphylinidae

Dyscolus reflexicollis (100)** Aleocharinae sp. 2 (100)** Uroxys sp. 5 (35)* Euspilotus sp.2 (85)** Aleochara notula (31)*

Dyscolus teter (100)** Anotylus sp. 1 (100)** Hister coenosus (50)** Tenebrionidae

Hydrophilidae Atheta sp. 1 (100)** Xerosaprinus sp.3 (36)** Tenebrionidae sp. 8 (30)*

Cercyon sp. 6 (100)** Atheta sp. 4 (100)** Leiodidae

Cercyon sp. 7 (100)** Belonuchus sp. 1 (100)** Dissochetus sp. 2 (33)**

Cercyon sp. 9 (75)** Diestota sp. 1 (100)** Nitidulidae

Leiodidae Diestota sp. 2 (100)** Stelidota sp. 2 (45)**

Dissochetus sp. 1 (100)** Falagria sp. 1 (100)** Scarabaeidae

Dissochetus sp. 4 (100)** Gnypeta sp. (100)** Uroxys sp. 1 (86)**

Ptomaphagus sp. (100)** Homalotini sp. (100)** Uroxys sp. 4 (75)**

Nitidulidae Hoplandria sp. (100)** Uroxys sp. 2 (41)*

Aethina villosa (100)** Myllaena sp. (100)** Staphylinidae

Epuraea sp. 1 (100)** Parocyusa sp. 1 (100)** Hoplandria peltata (92)**

Stelidota sp. 3 (100)** Parocyusa sp. 2 (100)** Belonuchus rufipennis (76)**

Stelidota sp. 4 (100)** Phloenomus sp. 1 (100)** Coproporus hepaticus (70)**

Stelidota sp. 5 (100)** Phylonthus sp. 2 (100)** Aleocharinae sp. 23 (45)*

Scarabaeidae Platydracus sp. 1 (100)**

Onthophagus cyanellus (100)** Quedius sp. (100)**

Other families Tinotus caviceps (100)**

Cryptophagidae sp. 3 (100)** Ocyota sp. 1 (75)**

Cryptophagidae sp. 4 (100)** Phylonthus sp. 1 (75)**

Ptiliidae sp. 1 (100)** Diestota sp. 3 (75)**

Scydmaenidae sp. 4 (100)** Ocyota sp. 2 (50)**

Tenebrionidae sp. 2 (75)** Phloenomus sp. 2 (50)**

Indicator value is given in parenthesis. Significance of Monte Carlo test: *P \ 0.05; **P \ 0.01

Names in bold denote beetle families

544 J Insect Conserv (2012) 16:537–547

123

ravines, and savannah (Ball and Bousquet 2001), being a

potential explanation an early emergence of Carabidae to

avoid competition with other groups of comparable feeding

preferences (Andresen 2005).

Second, seasonality had a profound effect on the struc-

ture of beetle assemblages: changes in diversity of necro-

philes were particularly dramatic from dry to wet seasons

(see Fig. 1b, g, h). However, while no changes in diversity

levels for coprophiles between seasons were distinguished,

both diversity and community structure differed signifi-

cantly among vegetation types between seasons. In this

sense, most of the information available for dung beetles

(dung and carrion Scarabaeidae beetles) suggests this group

to be particularly sensitive to habitat suitability (Hanski

and Cambefort 1991), as well as to experience significant

decreases in diversity in dry tropical areas with a pro-

nounced seasonality (Janzen 1983; Andresen 2005, 2008;

Mendes and Linhares 2006). Furthermore, we found a high

dominance and a low diversity in most stressful conditions:

during the dry season and in the most disturbed vegetation

type (the case for savannah). These findings are related to

the fact that many coprophilous communities tend to be

numerically dominated by a few species (Doube 1987), that

this pattern is relatively common in open and climatically

unstable habitats (Magurran 2004), and that this phenom-

enon has been recorded for dung beetles in other Neo-

tropical dry forests (Escobar 1997; Andresen 2005, 2008).

Third, our results suggest that vegetation type and

conditions play an important role for population persis-

tence, and particularly for specialist beetles. For instance,

relatively large tracks of forest (i.e. ‘‘Huitepec’’ site) con-

tained the highest diversity of necrophiles, very likely

because an important number of vertebrates occur there

(Naranjo and Espinosa-Medinilla 2003) and hence the

availability of carcasses might increase accordingly. Con-

versely, in fragmented tropical areas (like in San Fernando)

certain vegetation types such as ravines constituted

potential refuges for insect fauna. These results are in line

with previous findings with beetle groups in which certain

pieces of land represent key elements for population per-

sistence (Gibbs and Stanton 2001; Halffter and Arellano

2002; Caballero et al. 2009; Vasquez-Velez et al. 2010). In

these fragmented landscapes, carrion of small mammals,

amphibians, birds and reptilians—which tend to concen-

trate in oak forest remnants—became the primary source of

food for necrophile populations. However, this pattern does

not hold for coprophiles perhaps because a large number of

mammals in the Neotropics tend to be rather small (\2 kg)

and only producing small amounts of dung (Emmons

1997)—the establishment and free movement of cattle in

areas like San Fernando represent a relatively important

supply of dung (Arellano et al. 2008a). We must consider

though that deliberately offering of dung or carrion in the

field could potentially bias beetle attraction, which in turn

might inflate diversity levels for a given vegetation type i.e.

the supply of trap baits could have altered the movement

behavior of beetles as these insects are able to locate baits

from a distance. Nonetheless, we consider the amount of

dung or carrion used in the baits small compared to what is

naturally available in the landscape, and hence movements

and behavior of beetles through the landscape are relatively

unbiased (see Arellano et al. 2008b).

Overall, our data highlight the need to preserve few

large forest tracts and key vegetation types (such as

ravines); these pieces of land not only counteract the

adverse effects of habitat loss and the impacts of stressful

conditions caused by seasonality, but constitute the reser-

voir of key species that occur there: [41% of the necro-

phile indicator species are Staphylinidae associated to

relatively pristine oak forests. Whilst seasonality and

vegetation type are important predictors of beetle diversity,

(measured as density, evenness, and distinctiveness), con-

ditions during an extended dry period coupled with

anthropogenic pressures underline the fact that key vege-

tation types (e.g.[21% of coprophile indicator species are

Staphylinidae restricted to ravines) play important roles as

refugees for many beetle species. These pieces of land

provide a diverse array of habitats, landforms and com-

munities that are naturally rich in biodiversity (Corbacho

et al. 2003). In a wider context, the native oak forests of our

study area have undergone high rates of forest loss during

the last three decades (in the case of the ‘‘highlands of

Chiapas’’ exhibiting a deforestation rate of 3.4% per year;

Echeverria et al. 2007), compared to many other forested

landscapes in the world (Cohen et al. 2002; Staus et al.

2002). These forests have been reduced severely and

degraded over time owing to logging for timber and fuel

wood, clearance for cultivation, and quarry developments.

The worry is that previous surveys (including ours) have

demonstrated that these patchy oak forests still contain

unusual levels of biodiversity and many uniquely Mexican

taxa of plants and animals (Peterson et al. 1993), thus

fragmentation and loss of forests can broadly be expected

to lose substantial amounts of biodiversity over the long

term (e.g. Bawa and Seidler 1998).

Our studies clearly demonstrates that the least frag-

mented oak forest and ravine are the most valuable areas

for necrophile and coprophile beetles in Neotropical

Mexico, especially for specialist beetles. Fragmentation,

via land-use conversion associated with agriculture and

exploitation will have a negative impact on beetle diversity

and overall biodiversity within this Neotropical area.

Acknowledgments We are grateful to San Fernando landowners

and PRONATURA, the administrator of Huitepec Reserve, for

allowing access to field sites. Taxonomical identifications were

J Insect Conserv (2012) 16:537–547 545

123

confirmed by S. J. Ashe� (Staphylinidae), G. E. Ball (Carabidae), M.

S. Caterino (Histeridae), A. R. Cline (Nitidulidae), S. B. Peck (Lei-

odidae). Dolores Vidal (UNICACH) provided laboratory rats. Manuel

Giron, Arcangel Molina and Irma Miss helped in the field. Michael

Caterino, Jack Longino, Robert Anderson and two anonymous

reviewers provided useful comments on early versions of this paper.

Funding was provided by The National Council for Science and

Technology (CONACYT: Grants J35230-V, CHIS-2005-C03-054,

CONACYT-SEMARNAT 108222, PIFOP-ECOSUR, and PATM-

ECOSUR).

References

Andresen E (2005) Effects of season and vegetation type on

community organization of dung beetles in a tropical dry forest.

Biotropica 37:291–300

Andresen E (2008) Dung beetle assemblages in primary forest and

disturbed habitats in a tropical dry forest landscape in Western

Mexico. J Insect Conserv 12:639–650

Anonymous (2006) Temperatura y precipitacion media mensual

1951–2006. Estaciones meteorologicas Tuxtla Gutierrez (DGE)

y San Cristobal de las Casas (La Cabana) Chiapas. Mexico.

Comision Nacional del Agua, Chiapas

Arellano L, Leon-Cortes JL, Halffter G (2008a) Response of dung

beetle assemblages to landscape structure in remnant natural and

modified habitats in southern Mexico. Insect Conserv Divers

1:253–262

Arellano L, Leon-Cortes JL, Ovaskainen O (2008b) Patterns of

abundance and movement in relation to landscape structure: a

study of a common scarab (Canthon cyanellus cyanellus) in

Southern Mexico. Landscape Ecol 23:69–78

Arnett RH Jr, Thomas MC, Skelley PE, Frank JH (2002) American

Beetles, Volume II: Polyphaga: Scarabaeoidea through Curcu-

lionoidea. CRC Press, Boca Raton

Ball GE, Bousquet Y (2001) Carabidae. In: Arnett RH Jr, Thomas

MC (eds) American Beetles. Volume 1. Archostemata, Myx-

ophaga, Adephaga, Polyphaga: Staphyliniformia. CRC Press

LLC, Boca Raton, pp 32–131

Bawa KS, Seidler R (1998) Natural forest management and conser-

vation of biodiversity in tropical forests. Conserv Biol 12:46–55

Bernon G (1981) Species abundance and diversity of the Coleoptera

component of a South African cow dung community, and

associated insect predators. Ph D dissertation, University of

Bowling Green, USA

Borror DJ, Triplehorn CA, Johnson NF (1989) An introduction to the

study of insects. Saunders College Publishing, Philadelphia

Caballero U, Leon-Cortes JL, Moron-Rıos A (2009) Response of rove

beetles (Staphylinidae) to various habitat types and change in

Southern Mexico. J Insect Conserv 13:67–75

Carter DO, Yellowlees D, Tibbett M (2007) Cadaver decomposition

in terrestrial ecosystems. Naturwissenschaften 94:12–24

Chao A (2005) Species richness stimation. In: Balakrishnan N, Read

CB, Vidakovic B (eds) Encyclopedia of statistical sciences.

Wiley, New York, pp 7909–7916

Chao A, Chazdon RL, Colwell RK, Shen T-J (2005) A new statistical

approach for assessing similarity of species composition with

incidence and abundance data. Ecol Lett 8:148–159

Cohen WB, Spies TA, Alig RJ, Oetter DR, Maiersperger TK, Fiorella

M (2002) Characterizing 23 years (1972–95) of stand replace-

ment disturbance in western Oregon forests with Landsat

imagery. Ecosystems 5:122–137

Colwell RK (2009) EstimateS: Statistical estimation of species

richness and shared species from samples, (Software and User’s

guide), Version 8.2. Persistent Available from URL: http://purl.

oclc.org/estimates

Corbacho C, Sanchez JM, Costillo E (2003) Patterns of structural

complexity and human disturbance of riparian vegetation in

agricultural landscapes of a Mediterranean area. Agric Ecosyst

Environ 95:495–507

Costa C (2000) Estado de conocimiento de los Coleoptera Neotrop-

icales. In: Martin-Piera F, Morrone J, Melic A (eds) Hacia un

proyecto CYTED para el inventario y estimacion de la divers-

idad entomologica en Iberoamerica. Pri-Bes-2000.m3 m: Mo-

nografıas Tercer Milenio 1:99–114

Creighton JC, Bastarache R, Lomolino MV, Belk MC (2009) Effect

of forest removal on the abundance of the endangered American

burying beetle, Nicrophorus americanus (Coleoptera: Silphidae).

J Insect Conserv 13:37–43

Davis ALV (1994) Habitat fragmentation in southern Africa anddistributional response patterns in five specialist or generalist

dung beetle families (Coleoptera). Afr J Ecol 32:192–207

Davis ALV, Doube BM, Maclennan PD (1988) Habitat associations

and seasonal abundance of dung beetles (Coleoptera: Staphylin-

idae, Hydrophilidae, Histeridae) in the Hluhluwe region of South

Africa. Bull Entomol Res 78:425–434

Didham RK, Lawton JH, Hammond PM, Eggleton P (1998) Trophic

structure stability and extinction dynamics of beetles (Coleop-

tera) in tropical forest fragments. Philos T Roy Soc B 353:437–

451

Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu

Rev Environ Resour 28:133–167

Doube BM (1987) Spatial and temporal organization in communities

associated with dung pads and carcasses. In: Gee JHR, Giller PS

(eds) Organization of communities: past and present. British

Ecological Society symposium. Blackwell, Oxford, pp 255–280

Dufrene M, Legendre P (1997) Species assemblages and indicator

species: the need for a flexible assymetrical approach. Ecol

Monogr 67:345–366

Dunn RR, Danoff-Burg JA (2007) Road size and carrion beetle

assemblages in a New York forest. J Insect Conserv 11:325–332

Echeverria C, Cayuela L et al (2007) Spatial and temporal patterns of

forest loss and fragmentation in Mexico and Chile. In: Newton A

(ed) Biodiversity loss and conservation in fragmented forest

landscapes the forest of Montane Mexico and temperate South

America. CABI internacional, Wallingford, pp 14–42

Emmons LH (1997) Neotropical rainforest mammals: a field guide.

University of Chicago Press, Chicago

Escobar F (1997) Estudio de la comunidad de coleopteros coprofagos

(Scarabaeidae) en un remanente de bosque seco al norte del

Tolima, Colombia. Caldasia 19:419–430

Fahring L (2003) Effects of habitat loss and fragmentation on

biodiversity. Annu Rev Ecol Syst 34:487–515

Gibbs JP, Stanton EJ (2001) Habitat fragmentation and arthropod

community change: Burying beetles, phoretic mites and flies.

Ecol Appl 11:79–85

Gotelli N, Colwell RK (2001) Quantifying biodiversity: Procedures

and pitfalls in the measurement and comparison of species

richness. Ecol Lett 4:379–391

Halffter G, Arellano L (2002) Response of dung beetle diversity to

human-induced changes in a tropical landscape. Biotropica

34:144–154

Hanski I (1983) Coexistence of competitors in patchy environment.

Ecology 64:493–500

Hanski I (1987) Colonization of ephemeral habitats. In: Gray AJ,

Crawley MJ, Edwards PJ (eds) Colonization, succession and

stability. Blackwell, Oxford, pp 155–185

Hanski I, Cambefort Y (1991) Resource partitioning. In: Hanski I,

Cambefort Y (eds) Dung beetle ecology. Princeton University

Press, Princeton New Jersey, pp 330–349

546 J Insect Conserv (2012) 16:537–547

123

http://purl.oclc.org/estimates

http://purl.oclc.org/estimates

Holter P (1982) Resource utilization and local coexistence in a guild

of scarabaeid dung beetles (Aphodius spp.). Oikos 39:213–227

Hopp PW, Ottermanns R, Caron E, Meyer S, Roß-Nickoll M (2010)

Recovery of litter inhabiting beetle assemblages during forest

regeneration in the Atlantic forest of Southern Brazil. Insect

Conserv Divers 3:103–113

Janzen DH (1983) Seasonal changes in abundance of large nocturnal

dung beetles (Scarabaeidae) in Costa Rica deciduous forest and

adjacent horse pasture. Oikos 41:274–283

Klein B (1989) Effects of forest fragmentation on dung and carrion

beetle assemblages in central Amazonia. Ecology 70:1715–1725

Kocarek P (2000) A pitfall trap for ecology studies. Biol Bratislava

55:575–577

Kovarik PW, Caterino MS (2001) Histeridae. In: Arnett RH, Thomas

MC (eds) American Beetles, Volume 1. CRC Press, Boca Raton,

pp 212–227

Lamb D, Erskine P, Parrotta JA (2005) Restoration of degraded

tropical forest landscapes. Science 310:1628–1632

Magurran AE (2004) Measuring biological diversity. Blackwell

Publishing, Oxford

Mendes J, Linhares A (2006) Coleoptera associated with undisturbed

cow pats in pastures in Southeastern Brazil. Neotrop Entomol

35:715–723

Moore I (1954) An efficient method of collecting dung beetles. Pan-

Pac Entomol 30:208

Naranjo P, Espinosa-Medinilla E (2003) Los mamıferos de la reserva

ecologica Huitepec, Chiapas, Mexico. Rev Mex Mastozool

5:58–63

Navarrete–Heredia JL, Fierros–Lopez H (2001) Coleoptera de

Mexico: situacion actual y perspectivas de estudio. In: Navarr-

ete–Heredia JL, Fierros–Lopez H, Burgos–Solorio A (eds)

Topicos selectos sobre Coleoptera de Mexico. Universidad de

Guadalajara Jalisco/Universidad Autonoma del Estado de More-

los, Cuernavaca, pp 1–21

Nichols E, Larsen T, Spector S, Davis AL, Escobar F, Favila M,

Vulinec K (2007) Global dung beetle response to tropical forest

modification and fragmentation: a quantitative literature review

and meta-analysis. Biol Conserv 137:1–19

Novotny V, Basset Y (2000) Rare species in communities of tropical

insect herbivores: pondering the mystery of singletons. Oikos

89:564–572

Oliver I, Beattie AJ (1996) Invertebrate morphospecies as surrogates

for species: a case study. Conserv Biol 10:99–109

Parmenter RR, MacMahon JA (2009) Carrion decomposition and

nutrient cycling in a semi-arid shrub-steppe ecosystem. Ecol

Monogr 79:37–661

Payne JA (1965) A summer carrion study of the baby pig Sus scrofa

Linnaeus. Ecology 46:592–602

Peck SB (2001) Leiodidae. In: Arnett RH, Thomas MC (eds)

American Beetles, vol 1. CRC Press, Boca Raton, pp 250–258

Peterson AT, Flores-Villela A et al (1993) Conservation priorities in

Mexico: moving up in the world. Biodivers Lett 1:33–38

Pohl GR, Langor DW, Spence JR (2007) Rove beetles and ground

beetles (Coleoptera: Staphylinidae, Carabidae) as indicators of

harvest and regeneration practices in western Canadian foothills

forests. Biol Conserv 137:294–307

Putman RJ (1983) Carrion and Dung: the decomposition of animal

wastes. The Institute of Biology’s Studies in Biology No. 156,

Edward Arnold, London

Shorrocks B (1990) Coexistence in a patchy environment. In:

Shorrocks B, Swingland R (eds) Living in a patchy environment.

Oxford University Press, Oxford, pp 91–116

Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of

statistics in Biological Research, 3rd edn. WH Freeman and

Company, New York

Staus NL, Strittholt JR, Della-Sala DA, Robinson R (2002) Rate and

pattern of forest disturbance in the Klamath-Siskiyou ecoregion,

USA between 1972 and 1992. Landscape Ecol 17:455–470

Tokeshi M (1993) Species abundance patterns and community

structure. Adv Ecol Res 24:111–186

Trumbo ST, Bloch PL (2000) Habitat fragmentation and burying

beetle abundance and success. J Insect Conserv 4:245–252

Ulrich W, Komosinski K, Zalewski M (2008) Body size and biomass

distributions of carrion visiting beetles: do cities host smaller

species? Ecol Res 23:241–248

Vasquez-Velez L, Bermudez C, Chacon P, Lozano-Zambrano F

(2010) Analysis of the richness of Staphylinidae (Coleoptera) on

different scales of a sub-Andean rural landscape in Colombia.

Biodivers Conserv 19:1917–1931

Wolf JM, Gibbs JP (2004) Silphids in urban forests: diversity and

function. Urban Ecosyst 7:371–384

J Insect Conserv (2012) 16:537–547 547

123

High diversity beetle assemblages attracted to carrion and dung in threatened tropical oak forests in Southern Mexico

Documents