Differentiation in Searching Behavior for CarcassesBased on Flight Height Differences in Carrion Beetles(Coleoptera: Silphidae)

Hiroshi Ikeda & Satoshi Shimano & Akira Yamagami

Revised: 17 September 2010 /Accepted: 13 October 2010 /Published online: 4 November 2010# Springer Science+Business Media, LLC 2010

Abstract Flight ability allows insects to search for food and locate oviposition sitesacross a wide range of environments and, thus, allows insects to locate scarce andpatchy resources such as carcasses. We examined differentiation in searching forcarcasses, based on capture height differences in carrion beetles, and found thatcapture height differed among species. For Nicrophorus quadripunctatus andOiceoptoma nigropunctatum, the height of abundance peaks differed among sitesand was related to species composition at each site, indicating that shifts in flightheight can occur plastically, whereas those for Nicrophorus maculifrons andNicrophorus investigator did not differ among sites, indicating that the flightheights of these species are largely genetically determined. Thus, the presentdifferentiation in capture height is primarily determined by current plastic shifts andon some genetic basis.

Keywords Necrophagous .Nicrophorus . plasticity

Introduction

Flight allows insects to disperse over long distances and to search for food, partnersand oviposition sites across a wide range of environments. Previous studies have

J Insect Behav (2011) 24:167–174DOI 10.1007/s10905-010-9245-5

H. Ikeda (*)Department of Forest Entomology, Forestry and Forest Products Research Institute,1 Matsunosato Tsukuba, Ibaraki 305-8687, Japane-mail: hiroshiikeda@affrc.go.jp

S. ShimanoEnvironmental Education Center, Miyagi University of Education, 149 Aramaki, Aoba,Sendai city, Miyagi 980-0845, Japan

A. YamagamiLiberal Arts Education Center, Tokai University, 1117 Kitakaname, Hiratsuka city,Kanagawa 259-1292, Japan

demonstrated flight height differentiation related to food resources and ovipositionhabitats in butterflies (Devries and Walla 2001; Fermon et al. 2005), moths (Intachatand Holloway 2000; Brehm 2007) and wasps (Harrison 2003).

In carrion beetles (Coleoptera: Silphidae), most species use vertebrate carcasses asfood and breeding resources (e.g. Leschen 1993; Ratcliffe 1996; Eggert and Müller1997; Ikeda et al. 2007). Vertebrate carcasses are a scarce and patchy resource; thus,insects must search for carcasses on the fly. Ohkawara (1991) and Nagano andSuzuki (2003) elucidated the differentiation of searching behavior for carcasses viaflight height differences among sympatric species by examining capture heightdifferences. Ohkawara (1991) inferred that species flying at high heights broadlysearch for carcasses across a wide range, whereas species flying at low heights morefinely search across a narrow range.

Although Ohkawara (1991) and Nagano and Suzuki (2003) documented thedifferentiation through behavioral differences in Silphidae, their studies wereconducted at only one or two study sites; therefore, they were unable to determinewhether the capture height of each species was fixed or whether it can changeplastically. Plasticity can affect population dynamics by altering the interactionsbetween organisms and their abiotic and biotic environments and is thus importantfor stabilizing food webs (Miner et al. 2005). Fermon et al. (2005) demonstrated thatdifferences in the species richness of butterflies between natural and disturbed forestswere related to behavioral changes caused by variation in food resources andoviposition habitat. In Silphidae, capture height can change plastically, which maybe related to silphid species diversity. To address this issue, comparisons of captureheights must be made among sites that differ in species composition.

In this study, we examined the differentiation of capture height among sympatricsilphid species. Subsequently, we compared the differences in capture height of eachspecies among sites to reveal whether flight height can change plastically due tovariation in species composition.

Material and Methods

Our study was conducted at seven forest sites (Omotefuji: 35.37°N, 138.81°E, beechforest; Kiso: 35.83°N, 137.86°E, riparian deciduous forest; Sugadaira: 36.51°N,138.36°E, larch plantation forest; Kakuma: 36.45°N, 138.36°E, riparian forest;Inabu: 35.20°N, 137.57°E, cedar plantation forest; Baraki: 36.55°N, 138.47°E,deciduous forest; Madarao: 36.83°N, 138.30°E, deciduous forest) in Japan. Quercuscrispula dominated the deciduous forests of Kiso and Madarao, and Q. crispula andBetula platyphylla dominated those of Baraki. Sampling was conducted in July 1995at Omotefuji, Kiso, and Sugadaira; in July 1990 at Kakuma; in August 1995 atInabu; from July to August 1994 and 1995 at Baraki; and in August 1992 atMadarao. For Baraki, data were pooled for 1994 and 1995 because the patterns didnot differ between years. Beetles were collected using traps constructed of cans withchicken meat as bait (Fig. 1). Traps were set at five different heights (0, 0.5, 1.5, 4,and 8 m above the ground) for 3–6 days, and 20 replicates of these five-trap setswere hung or set on the ground at each site (100 traps/site). For traps at some sites,the internal cans were placed upside down to prevent damage by birds and

168 J Insect Behav (2011) 24:167–174

mammals. Carrion beetles are attracted by bait, so not all the collected individualsflew at their capture height. However, we used trap sets of five different heights inthe same place, with the only difference within a trap set being height. Thus, most ofthe individual insects flying around the trap height were expected to be trapped. Forthis reason, the data from our study represent the distribution pattern along height tosome degree.

We conducted two-sample Kolmogorov–Smirnov tests to examine differentiationof capture height among silphid species at each site. We used only those species withmore than five individuals at each site for analysis. We also performed two-sampleKolmogorov–Smirnov tests to examine the differences in capture height among sitesfor each species. For this analysis, we used only those species for which more thanfive individuals were collected at two or more sites.

Results

We collected 1,479 individuals from nine silphid species (Table 1). Species richnessvaried from two to eight species among sites. Capture height was differentiatedamong species in five natural and plantation forest sites (Omotefuji, Kiso, Sugadaira,Kakuma, and Madarao; Tables 1 and 2). Nicrophorus quadripunctatus, Nicrophorusmaculifrons, Nicrophorus investigator, and Oiceoptoma nigropunctatum wereprimarily collected at 0–4, 8, 4–8, and 0–4 m, respectively. Calosilpha brunnicolliswas found with equal proportion at all heights except 0 m. We were unable todetermine the patterns of capture heights for Nicrophorus concolor, Ptomascopusmorio, Dendroxena sexcarinata, and Necrodes littoralis due to small sample sizes.At most sites, capture heights differed significantly between those species searchingprimarily at low heights (N. quadripunctatus and O. nigropunctatum) and thosesearching primarily at high heights (N. maculifrons and N. investigator; Table 2).Furthermore, capture heights significantly differed at most sites between the twospecies searching at low heights (N. quadripunctatus and O. nigropunctatum),whereas capture heights did not differ between the two species primarily searching athigh heights (N. maculifrons and N. investigator).

Fig. 1 Conceptual diagram ofone set of five traps

J Insect Behav (2011) 24:167–174 169169

Tab

le1

Vertical

distributio

nof

silphidbeetlesat

each

studysite.The

ratio

ateach

height

andthetotalnumberin

each

speciesareshow

n

Height(m

)Omotefuji

Kiso

Sugadaira

Kakum

a

Nq

Nm

Ni

Nc

Nq

Nm

Ni

Nc

On

Nq

Nm

Ni

On

Nq

Nm

Ni

Nc

Pm

8.0

0.21

0.38

0.20

0.00

0.18

0.25

0.33

0.50

0.18

0.00

0.22

0.33

0.00

0.10

0.45

0.48

0.33

0.00

4.0

0.16

0.14

0.20

0.00

0.16

0.00

0.67

0.00

0.07

0.00

0.33

0.00

0.00

0.18

0.23

0.26

0.00

0.00

1.5

0.27

0.17

0.40

0.00

0.23

0.50

0.00

0.25

0.46

0.32

0.44

0.50

0.00

0.17

0.23

0.11

0.00

0.00

0.5

0.23

0.18

0.20

0.00

0.23

0.25

0.00

0.00

0.18

0.32

0.00

0.17

0.00

0.15

0.09

0.04

0.67

0.50

0.0

0.12

0.13

0.00

1.00

0.20

0.00

0.00

0.25

0.10

0.36

0.00

0.00

1.00

0.39

0.00

0.11

0.00

0.50

Total

317

785

344

49

414

753

96

1410

422

273

2

Heigh

t(m

)Kakum

aInabu

Baraki

Madarao

On

Cb

Ds

Nq

Nc

Nq

Nm

Ni

Nc

On

Cb

Nl

Nq

Nm

Ni

Nc

On

8.0

0.11

0.25

0.00

0.04

0.60

0.00

0.29

0.33

0.00

0.00

0.00

0.00

0.02

0.28

0.00

0.00

0.00

4.0

0.30

0.25

0.00

0.31

0.00

0.15

0.00

0.33

0.00

0.04

0.50

0.00

0.07

0.39

0.00

0.00

0.00

1.5

0.24

0.25

0.00

0.45

0.20

0.24

0.57

0.00

0.67

0.19

0.25

0.00

0.26

0.17

1.00

1.00

0.00

0.5

0.20

0.25

0.00

0.21

0.00

0.22

0.14

0.33

0.33

0.22

0.25

0.00

0.28

0.09

0.00

0.00

0.11

0.0

0.15

0.00

1.00

0.00

0.20

0.39

0.00

0.00

0.00

0.56

0.00

1.00

0.36

0.07

0.00

0.00

0.89

Total

190

161

150

567

73

327

41

9646

21

9

NqNicroph

orus

quad

ripunctatus,Nm

N.m

aculifron

s,NiN

.investig

ator,N

cN.con

color,OnOiceoptom

anigrop

unctatum

,Pm

Ptomascopusmorio,C

bCalosilp

habrunnicollis,

DsDendroxenasexcarinata,

NlNecrodeslittoralis

170 J Insect Behav (2011) 24:167–174

Four species (N. quadripunctatus, N. maculifrons, N. investigator, and O.nigropunctatum) were used to analyze differences in capture height among sites.Capture heights differed among sites for N. quadripunctatus and O. nigropunctatumbut not for N. maculifrons and N. investigator (Table 3). For N. quadripunctatus,most comparisons between sites were significant. Although N. quadripunctatus wascollected primarily at relatively low heights, the height of peak abundance variedamong sites from 0 m at Kakuma and Madarao to 0.5–1.5 m at Omotefuji and1.5–4 m at Inabu. For O. nigropunctatum, most comparisons between sites were alsosignificant. This species was collected primarily at relatively low heights, but theheight of peak abundance ranged from 0 m at Sugadaira and Madarao to 1.5 m atKiso and 4 m at Kakuma.

Discussion

Our study demonstrated that the heights of peak abundance varied significantlyamong sites for N. quadripunctatus and O. nigropunctatum. Such differences werenot related to forest type. Our results indicated that shifts in capture height can occurplastically. The distribution of capture heights for N. quadripunctatus and O.nigropunctatum appeared to be related to one another. The height of peak abundanceof N. quadripunctatus was 0.5 m at sites in which O. nigropunctatum was absent(Omotefuji and Inabu), whereas it was 0 m or unclear, and the total abundance of N.quadripunctatus was relatively low at sites with relatively high abundances of O.nigropunctatum (Kiso and Kakuma). Considering that N. quadripunctatus and O.nigropunctatum both exhibited high densities at relatively low heights, interspecificinteractions between the two species may induce a shift in capture height atrelatively low heights.

Although we observed shifts in capture height for N. quadripunctatus and O.nigropunctatum, these two species were primarily collected at low heights.Furthermore, plastic shifts in capture height did not appear to occur in N.maculifrons and N. investigator. Thus, a portion of the current differentiation ofcapture height among silphid species was likely genetically determined.

Table 2 Differentiation of flight height among species within each site

Nm Ni Nc On Cb

Nq O, S, Ka, B, M O, Ki, S, Ka I Ki, S, Ka, B, M Ka

Nm O, S, Ka – S, Ka, B, M Ka

Ni – Ki, S, Ka Ka

Nc – –

On Ka

Sites for which flight heights significantly varied among species are indicated by italics (P<0.05) or bold italics(P<0.01). O Omotefuji; Ki Kiso; S Sugadaira; Ka Kakuma; I Inabu; B Baraki; M Madarao. Abbreviations for speciesnames are as shown in Table 1

J Insect Behav (2011) 24:167–174 171171

Ikeda et al. (2006) demonstrated a relationship between body size and food andbreeding resources among Nicrophorus species. In addition, Ohkawara (1991) notedthat larger species tend to fly at a higher stratum than smaller species. Therefore,differences in body size due to interspecific differences in food and breeding resourceuse may be related to interspecific differences in capture height. In this study, we did notexamine the relationship between body size and capture height because of small samplesizes for large Nicrophorus species as well as the absence of small-sized species.Further studies should more thoroughly investigate these relationships.

Most previous studies of carrion beetle communities use pitfall traps on theground (Katakura and Fukuda 1975; Katakura et al. 1986; Katakura and Ueno 1985;

Table 3 Results of two-sample Kolmogorov–Smirnov tests among sites for species searching primarily atlow heights (a: N. quadripunctatus, b: O. nigropunctatum) and for species primarily searching at highheights (c: N. maculifrons, d: N. investigator)

Kiso Sugadaira Kakuma Inabu Baraki Madarao

a

Omotefuji 0.08 0.37 0.27 0.17 0.27 0.29

Kiso 0.34 0.19 0.23 0.19 0.25

Sugadaira 0.28 0.47 0.15 0.09

Kakuma 0.39 0.13 0.19

Inabu 0.41 0.44

Baraki 0.06

b

Omotefuji – – – – – –

Kiso 0.90 0.15 – 0.50 0.79

Sugadaira 0.85 – 0.44 0.11

Kakuma – 0.43 0.74

Inabu – –

Baraki 0.33

c

Omotefuji – 0.31 0.22 – 0.24 0.16

Kiso – – – – –

Sugadaira 0.23 – 0.27 0.15

Kakuma – 0.40 0.17

Inabu – –

Baraki 0.39

d

Omotefuji 0.60 0.13 0.34 – – –

Kiso 0.67 0.26 – – –

Sugadaira 0.41 – – –

Kakuma – – –

Inabu – –

Baraki –

Significant results are indicated by italics (P<0.05) or bold italics (P<0.01)

172 J Insect Behav (2011) 24:167–174

Martin 1989; Ohkawara et al. 1998). However, we demonstrated that some speciesfly at high heights, whereas others fly at low heights. Therefore, sampling data frompitfall traps on the ground at forest sites may underestimate the population size ofcarrion beetle species that fly at high heights, such as N. maculifrons andN. investigator.

Although all carrion beetles examined in this study make use of vertebratecarcasses on the ground, the ability to search for carcasses above ground level wasdifferent among species and the flight height of some species shifted plastically,related to species composition. The difference in flight height may be related to otherflight behavioral patterns and the targeting carrion type. Further study will revealsuch differentiation related to flight height.

Acknowledgments This research was supported by a grant-in-aid from the Japan Society of Promotionof Sciences (No. 20579001).

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