A review of hypotheses of decline of the endangered American buryingbeetle (Silphidae: Nicrophorus americanus Olivier).

Derek S. Sikes1 and Christopher J. Raithel2,*1Department of Ecology & Evolutionary Biology, University of Connecticut, U-43, Storrs, CT 06278, USA;2RI Department of Environmental Management, Division of Fish & Wildlife, PO Box 218, West Kingston,RI 02892, USA; *Author for correspondence (e-mail: craithel@mindspring.com; phone: 401-789-0281; fax:401-783-7490)

Received 19 October 2001; accepted in revised form 5 March 2002

Key words: American burying beetle, Endangered species, Hypotheses of decline, Nicrophorus americanus, Sil-phidae

Abstract

The largest species of North American Nicrophorus (Coleoptera: Silphidae), N. americanus, was placed on theUS federal list of endangered species in 1989. This paper reviews literature bearing on eight hypotheses thatattempt to explain the dramatic decline of this species over 90% of its former range. What is known regardingeach hypothesis is separated from what remains to be investigated. We find that although progress has been madeduring the past 12 years, even the most well supported hypothesis requires a number of important studies to becompleted or extended before we can confidently explain the decline of this species and predict the success ofconservation efforts.

Introduction

The American burying beetle, Nicrophorus america-nus Olivier, was first listed as endangered in 1989 bythe US Fish and Wildlife Service (Federal Register54(133): 29652–55), after museum and field surveysin the early 1980s discovered it was absent from mostof its historic range (Davis 1980; Anderson 1982).This species has been the subject of intense study andspeculation since its decline was announced in 1980.We have found 46 papers published during the first200 years before 1980 that referred to this species(usually providing minimal ecological information),but in the last twenty years an additional 78 publica-tions have appeared, most of which focused on thisspecies (Sikes et al. 1999), but none of which an-swered the central question of what caused this spe-cies’ decline.

In North America north of Mexico, and exclusiveof the West Indies, there are 15 species of Nicropho-rus (Peck and Kaulbars 1987; Sikes and Peck 2000).These beetles are popular among biologists because,

in addition to their large size and colorful markings,they exhibit complex reproductive behaviors, includ-ing biparental care, which is extremely rare in the or-der Coleoptera. They derive their common name,burying beetles, from their habit of burying small ver-tebrate carcasses, on which they raise their offspring.The ecology and behaviors of over 20 Nicrophorusspecies have been well studied (Pukowski (1933) andTrumbo (1992), Scott (1998), Sikes et al. (1999) andreferences therein). Kozol et al. (1988) were the firstto publish a detailed life history of N. americanus.

As recently as the 1920s, Nicrophorus americanuswas considered common across most of the easternhalf of North America and was known from 35 statesand three Canadian provinces (Davis 1980; Anderson1982). However, it now occurs in less than 10% ofits former range (Figure 1). Populations are restrictedto Block Island, Rhode Island, an island off the At-lantic coast, and the western periphery of the historicrange (western Arkansas, eastern Oklahoma, centraland southern Nebraska, southeastern Kansas, andsouthcentral South Dakota). Wells et al. (1983) stated

103Journal of Insect Conservation 6: 103–113, 2002.© 2002 Kluwer Academic Publishers. Printed in the Netherlands.

that this species’ case “must represent one of the mostdisastrous declines of an insect’s range ever to be re-corded.” This dramatic example of species endanger-ment is unusual in that it is difficult to imagine ascenario that would drive N. americanus, which isphysically dominant within its guild, to the brink ofextinction yet leave its eight sympatric congeners un-touched.

Many hypotheses for this decline have been sug-gested; only some of which have been explored em-pirically, and none exhaustively (Table 1). The deter-mination of why this species has declined depends tosome extent on knowing what factors predict its pres-ence. However, the factors that led to the decline ofN. americanus may not all still be present. If formerlimiting factors no longer occur, then we might ex-pect N. americanus to gradually expand back into itshistoric range, but there is no evidence that this ishappening. If the factors that led to the decline of thisspecies continue to shape its current distribution andprevent recolonization of former habitats, then weshould be able to determine precisely what these fac-tors are. Although there is a large body of circumstan-

tial evidence, much of which has been cited in priordiscussions of this species’ decline, there remain nu-merous questions to be answered and suppositions tobe supported by empirical evidence. Without this in-formation firmly in hand, conservation efforts arehandicapped.

Herein we will briefly present the hypotheses ofdecline for N. americanus and discuss what has beenlearned during the last twelve years about each.

It should be mentioned that each hypothesis in Ta-ble 1 is not exclusive of the others. In fact, it is likelythat multiple effects interacted, perhaps synergisti-cally, to influence the decline of N. americanus (My-ers 1987; Ratcliffe 1995; Amaral et al. 1997). How-ever, any explanation for the decline of N. americanusmust at least address why the sympatric congeners,which feed and breed on similar resources, have ap-parently remained unaffected.

DDT/pesticide use

Kozol (1995), and Raithel (in US Fish and WildlifeService (1991)), presented a clear argument against

Figure 1. Current (black) and historic (gray shade and white dots) range of N. americanus (modified from Lomolino et al. (1995) and Hol-loway and Schnell’s (1997), US Fish and Wildlife Service (1991).

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the DDT hypothesis, pointing out that the Americanburying beetle had disappeared from areas whereDDT was never sprayed, that some recent (since1960) populations were in areas that had been sprayedwith DDT, and that most populations were gone 25years before DDT, or other organochlorine pesticides,were used. Raithel (US Fish and Wildlife Service1991) pointed out, however, that several N. america-nus populations in the Midwest did disappear duringthe period that DDT was applied (1940 to 1972).Also, in a controlled study of the effects of DDT onforest invertebrates, Hoffmann et al. (1949) showedthat DDT spraying eliminated populations of threeNicrophorus species (Nicrophorus orbicollis Say,Nicrophorus sayi Weber, and Nicrophours defodiensMannerheim). Irrespective of the pattern and timingof decline, for DDT, or any man-made toxin, to be asignificant factor in this puzzle we would have toevoke ad hoc hypotheses to account for the lack ofequivalent impact on the sympatric congeners of N.americanus. Unfortunately, there are few historicaldata (e.g., Trumbo and Thomas (1998)) regardingNicrophorus community structure with which to as-sess effects of past DDT spraying or other contami-nants. Although this hypothesis is rejected as the pri-mary explanation, it remains possible that some N.americanus, and presumably other Nicrophorus, pop-ulations may have been extirpated by DDT use.

Artificial lighting

Artificial lighting as an explanation of decline (e.g.,Ratcliffe (1995, 1996)) is less easily dismissed. Sev-eral extant populations of the American burying bee-tle do occur in remote, relatively lightless areas. The

responses of silphids to artificial lights vary amongspecies. Backlund and Marrone (1997) captured 13species of silphid in baited pitfall traps in south-cen-tral South Dakota, but only three species were com-mon at black lights. They captured no N. americanusat lights during their sampling but did catch this spe-cies in pitfall traps. In the Northeast, N. americanus(US Fish and Wildlife Service 1991), as well as N.orbicollis, N. pustulatus Herschel, and Necrodes suri-namensis (Fabricius), consistently come to lights(Anderson and Peck 1985). However, N. americanusis attracted less frequently to lights than to carrionbaited traps. Even in the areas of Block Island wherethe American burying beetles are most common, it istypical to see only a few (0–3) individuals per nightat a blacklight.

There are few empirical data that quantify lightcaptures for this species. Circumstantial support forartificial lights as a factor in the decline could be de-rived from the fact that most extant populations of N.americanus occur in relatively remote, lightless areas,and electric lighting was becoming widespread dur-ing the late 1800s (Bright 1949), concurrent with thebeginning of N. americanus’ disappearance from theNortheast. However, fluorescent lights (includingblacklights like those used in “Bug Zappers”) are con-siderably more attractive to night-flying insects, andthese are a relatively recent feature of the landscape.Additionally, the N. americanus population on BlockIsland has coexisted with artificial light for over 50years and both N. orbicollis and Necrodes surinamen-sis, other light-attracted silphids, remain abundantthere.

This hypothesis could be carefully addressedthrough studies that quantify the amount of artificial

Table 1. Hypotheses of decline for Nicrophorus americanus. See text for detailed description of each hypothesis. Accounts for congeners:does the hypothesis explain why sympatric congeners are unaffected? Accounts for pattern: does the hypothesis explain the geographicpattern (Figure 1).

Hypothesis source accounts for congeners? accounts for pattern?

DDT/pesticide use (Kozol et al. 1988) no no

Artificial lighting (Ratcliffe 1995) no no

Pathogen (US Fish and Wildlife Service 1991) yes yes

Habitat alteration hypotheses:

Old growth specialist (Anderson 1982) yes no

Prairie specialist (herein) yes yes

Vertebrate competition (US Fish and Wildlife Service 1991) yes no

Loss of ideal carrion (US Fish and Wildlife Service 1991) yes no

Congener competition (US Fish and Wildlife Service 1991) yes no

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light near the extant populations, and examine themortality of N. americanus and congeners due tothese lights. It remains at least possible that artificiallights, if they are responsible for a chronic, albeit low,level of adult attrition, could be affecting N. america-nus populations. Nevertheless, it presently seems thatif artificial lighting has had a negative effect on N.americanus, it has been minor relative to other influ-ences.

Pathogen

In addition to accounting for the health of sympatriccongeners, a good hypothesis should also explain theunusual geographic pattern of the remaining popula-tions (Figure 1). It is a widely held belief that spe-cies’ ecological requirements are best met toward thecenters of their distributions. However, N. america-nus disappeared from its range core and persists onlyon the very edge of its historic range.

A pathogen hypothesis readily accounts for such ageographic pattern of decline. Any pathogen thatcould be transmitted among adult burying beetles, andwas non-fatal to congeners of N. americanus, wouldeliminate all contiguous N. americanus populations,leaving only peripheral isolates untouched. Raithel (inUS Fish and Wildlife Service (1991)) suggested thishypothesis and also pointed out that no evidence of adisease or pathogen has been found. However, weknow of no investigation that expressly attempted totest this hypothesis. Consistent with this theory is thephylogenetic analysis of Peck and Anderson (1985)in which N. americanus was not found to belong toany of the Nicrophorus species groups of the NewWorld, i.e., it was phenotypically, and presumablyevolutionarily, distant. Nicrophorus americanus,therefore, could be physiologically unique and vul-nerable to a pathogen to which its congeners are im-mune. The numerous Nicrophorus symbionts, whichinclude mites and nematodes, could also contribute tothe spread of disease. These symbionts rapidly trans-fer among hosts, both within and among species,when the beetles feed at carcasses too large to bury(Schwarz and Koulianos 1998).

Channel and Lomolino (2000), investigated thegeographic pattern of decline in 245 endangered spe-cies. Their analysis showed that the remaining popu-lations of many endangered species (98% of theirsample), including birds, mammals, fishes, mollusks,arthropods, and plants, are in the peripheries of theirformer ranges. Therefore, the peripheral isolate pat-

tern noted for N. americanus may be the rule ratherthan the exception. They suggested that this patternresulted from the “contagion-like spread of extinctionforces” (loc. cit.), primarily a loss of ideal habitatfrom the center of a species range. Since this geo-graphic pattern of decline has been observed in caseswhere pathogens were not involved, an explanationfor the observed pattern of decline of N. americanusdoes not necessarily depend on an epizootic event.However, Channel and Lomolino’s (2000) investiga-tion certainly does not eliminate the possibility thatsome sort of pathogen may have affected N. ameri-canus populations.

Habitat loss

The remaining hypotheses deal primarily withchanges to the habitat of N. americanus, including thecarrion resource base. However, data that address dif-ferences between the central and the peripheral habi-tats of N. americanus’ historic range are still lacking.Although these hypotheses are plausible and accountfor the persistence of sympatric congeners, they donot definitively explain how the current geographicpattern (Figure 1) was created.

Vegetation changes: old growth specialist

The very first hypothesis published to explain the de-cline of N. americanus was that of Anderson (1982),who suggested that the species might be a specialistof old growth forests and require the deeper, loosersoils of such habitats. There are indications that N.americanus formerly occurred in primary forests. Forexample, Walker (1952) described a capture site inTennessee as an open “park-like” forest with thickherbaceous vegetation and Creighton et al. (1993)showed this species to be more common in open, up-land forests and grasslands than in densely vegetatedlowland forests. However, given the broad historicalrange of this species (Figure 1), it seems unlikely thatN. americanus could have been a vegetation special-ist. Lomolino et al. (1995) specifically tested and re-jected Anderson’s old growth hypothesis, concludingthat N. americanus was a vegetation generalist. Thereis information to indicate that N. americanus toler-ates, and may even prefer, open habitats. Most of thehistorical N. americanus collections, at least in theeastern portion of its range, occurred during the pe-riod when much of the landscape was highly agricul-tural. For example, Block Island was a thoroughly

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denuded sheep pasture for at least 200 years; todayits vegetation consists of maritime shrub communi-ties, coastal moraine grasslands and agricultural pas-tures. On Block Island, trap transects for N. america-nus are more successful in open areas (Raithel unpub.data). Western populations also occur in prairie andgrazed areas (Bedick et al. 1999), forest edge, opensavannah-like forests, and scrublands.

However, Lomolino and Creighton’s (1996), in an-other study designed to test Anderson’s hypothesis,found evidence that N. americanus preferred matureforests over clearcuts and had greater breeding suc-cess in forests relative to grasslands. They thoughtthis result might relate to the difficulty the beetlesfaced in burying carcasses in the grassland soils. Thedifference in productivity was due primarily to fail-ure rates in the grasslands; once buried, grassland car-casses produced similar larval complements as forestcarcasses. However, their emphasis on vegetationtype did not preclude other causes of burial failuresuch as ants or extreme temperature. A study focus-ing on vegetation alone may obscure two far moreimportant limiting factors; namely, vertebrate (and in-vertebrate) competition and the natural carrion preybase. In summary, testing for habitat preferencesbased on vegetation and soil type while ignoring boththe naturally occurring abundance of appropriatelysized carrion and the intensity of competition in eachhabitat type, could be misleading in the process ofidentifying limiting factors for N. americanus. Workdone on Block Island (Raithel in press) and in Arkan-sas (Holloway and Schnell’s 1997) suggests that veg-etation type might be a less efficient predictor of op-timal beetle habitat than the prey base and potentialvertebrate competition. Additional work, specificallyaddressing breeding success, including location suc-cess (i.e., where do beetles find more carcasses, sensuTrumbo and Bloch (2000)) and the naturally occur-ring prey base rather than trap captures or vegetationtype, is clearly required before we can determinewhat factors describe this species’ preferred habitat.

Vegetation changes: prairie specialist

An unpublished hypothesis, nearly opposite to theprevious, is that the decline of N. americanus may belinked to the return of forests in eastern North Amer-ica. If this species was ancestrally rare or absent inforests and preferred open habitats (as it does to somedegree today (Kozol et al. 1988; Lomolino et al.1995; Bedick et al. 1999)), its range may have ex-

panded during the agricultural deforestation of east-ern North America begun by native Americans andgreatly expanded by European settlers into the mid1800s (Askins 1997). Such an invasion of the eastern“neosavanna” has been documented for various grass-land associated bird species (US Fish and WildlifeService 1991). With the shift of agriculture from theeast to the west and the ensuing reforestation duringthe 1900’s, one might expect grassland-associatedspecies to disappear from many of the areas they hadfirst invaded perhaps centuries earlier. This pattern ofdecline and range retraction has been documented forseveral vertebrates associated with open, early suc-cessional habitats. For example, the New EnglandCottontail (Sylvilagus transitionalis) has disappearedfrom over 80% of its former range in the northeast-ern United Stattes (Litvaitis et al. 1999), and there arenumerous similarly declining birds (e.g., Bell’s Vireo[Vireo bellii], Painted Bunting [Passerina ciris])(l.c.).Therefore, the current distribution of N. americanusmight be closer to its pre-settlement distribution thanour collection record of the last 200 years would leadus to believe. An alternative explanation for a currentprairie association might involve a habitat switch inwhich the beetle, which once was abundant in forests,perhaps due to a constant supply of passenger pigeoncarcasses, is now only found in open habitats becauseof a dependence on the ground nesting birds or othersuitable carrion producers that prefer these habitats.

Holloway and Schnell’s (1997) and Lomolino andCreighton’s (1996) work, as with the previous hypo-thesis, indicate that this species can be captured inforests that contain enough of the correct sized car-rion. We should not, therefore, expect this species tobe a specialist of any particular vegetation type, nei-ther old growth forests nor prairies. It is logical thatthe carrion resource base is a significantly more im-portant predictor of healthy N. americanus popula-tions than any particular vegetation type.

Vertebrate competition

Raithel (US Fish and Wildlife Service 1991) con-cluded that the best explanation for the decline of N.americanus involved habitat fragmentation, which re-duced the carrion prey base and increased the verte-brate scavenger competition for it. Kozol (1995) andRatcliffe (1996), Amaral et al. (1997), Bedick et al.(1999), and other authors have reiterated this theme.

Nicrophorus americanus is the largest species ofNicrophorus in the New World and requires carcasses

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of 100–200 g (Kozol et al. 1988) to maximize its fe-cundity, whereas all other Nicrophorus species canbreed abundantly on much smaller carcasses, with thesmallest species using carcasses of 3–5 g (Trumbo1992). Potential scavenging, predatory, vertebratecompetitors of N. americanus include the AmericanCrow (Corvus brachyrhynchos), Red Fox (Vulpesvulpes), Striped Skunk (Mephitis mephitis), Raccoon(Procyon lotor), Norway Rat (Rattus norvegicus), Fe-ral Cat (Felis catus) (Jurek 1994), and two recent ad-ditions to the northeastern North American fauna: theCoyote (Canis latrans) (Parker 1995) and the VirginiaOpossum (Didelphis marsupialis). A number of thesespecies, especially the Raccoon and Striped Skunk,have seen dramatic population increases over the lastcentury (Garrott et al. 1993). The Coyote was rarelyfound outside of grassland habitats prior to the 20th

century, but with competitive release due to the extir-pation of larger predators, like the Gray Wolf (Canislupus) and the Mountain Lion (Felis concolor), theincrease in deer population, and changes in habitatusage throughout the northeast, the Coyote expandedits range into the forested northeast, reaching Ontarioin 1919 and Newfoundland in the 1990s (Gipson andBrillhart 1995; Parker 1995). Coyotes tend to be morecommon in open habitats than forests (Whitaker andHamilton 1998) – the same habitats that are preferredby various large, ground-nesting birds, which are bothexperiencing population declines and are potentialoptimally-sized carrion producers for the Americanburying beetle.

There is evidence to support a direct correlationbetween edge, or fragment size, and vertebrate scav-enger pressure, with much of this work involvingnesting bird populations (Paton 1994; Yahner and Ma-han 1996; Suarez et al. 1997). Some studies have ex-amined the effects of fragmentation on beetle com-munities (e.g., Klein (1989) and Trumbo and Bloch(2000)), but more studies of this phenomenon usingburying beetle communities are needed. Trumbo andBloch (2000) investigated the influence of fragmentsize on Nicrophorus species’ success (measured as theproportion of mouse carcasses buried and held forseven days). They found that beetles had significantlygreater success in larger woodland plots and attrib-uted this result in part to lower vertebrate scavengersuccess in those areas. Sikes (1996), working withNicrophorus nigrita Mannerheim, found that mousetransects laid > 100 m from a trail or road had 10%or fewer carcasses taken by vertebrates, whereastransects near trails or roads had an average of 85%

of the carcasses taken by vertebrate scavengers. Otherworkers, such as Wilson and Fudge (1984), haveshown that in sites with greater vertebrate scavengerpressure, variation in Nicrophorus brood size in-creased.

Trumbo and Thomas (1998) investigated Nicro-phorus species composition (lacking N. americanus)on several small islands and found that smaller is-lands were not able to support viable populations oflarge-bodied species. They suggested that larger spe-cies required more carrion resources and were there-fore more prone to local extinctions. The extant pop-ulation of N. americanus on Block Island seems to berelatively free of competitive pressures; not only arethere unusually large populations of ground-nestingbirds, but there are few mammal predators or scaven-gers (Amaral et al. 1997; Raithel in press). This hypo-thesis is among those most well supported by theavailable evidence. However, more studies on the re-sponse of silphid communities to habitat fragmenta-tion are needed, especially those that would contrasthistoric and current habitats, or compare multiple ex-tant sites of N. americanus.

Loss of ideal carrion

Raithel (loc. cit.) strengthened the explanatory powerof the vertebrate competition hypothesis by combin-ing it with another hypothesis–loss of carrion of idealsize. At least one bird species in the ideal weightrange and the historical geographic range of N. amer-icanus, the Passenger Pigeon (Ectopistes migratorius)is extinct. This species was historically one of themost abundant birds in North America, with flocksestimated to contain billions of individuals, (Wen-ninger 1910) and certainly would have produced asignificant amount of necromass during the reproduc-tive season of N. americanus. In addition, other birdspecies of the ideal weight size have declinedthroughout their ranges during the last century. Theseinclude the exotic Ring-necked Pheasant (Phasianuscolchicus), (Raithel in press) and other gallinaceousbirds like the Greater Prairie Chicken (Tympanuchuscupido), and the Northern Bobwhite (Colinus virgin-ianus), (Guthery et al. 2000). Raithel (in press) dem-onstrated that Block Island has a greater proportionof potential carrion producers (nesting birds, such asthe Ring-necked Pheasant and the American Wood-cock [Scolopax minor]) than the adjacent mainland.Holloway and Schnell’s (1997) study is the only oneconducted in the western portion of N. americanus’

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range that examined the carrion resource base. Theyfound significant correlations between the numbers ofN. americanus caught in traps and the biomass ofmammals, the biomass of mammals plus birds, thenumber of mammal species, and the number of indi-vidual mammals, irrespective of the predominant veg-etation.

However, we are terribly ignorant about what fac-tors determine the usefulness of a vertebrate speciesto N. americanus. We know little more than the idealweight of carrion and the presumed breeding seasonfor beetle reproduction–data regarding the localitiesfor suitable vertebrate populations, their mortalityrates, the process of carcass production and its quan-tity (and variance), and competition for carrion aregenerally lacking. Such data are required to build arobust population model for N. americanus. Educatedguess work indicates that ideal vertebrate species fora N. americanus prey base would be those that pro-duce ample offspring, many of which die after achiev-ing a mass of 80–200 g due to causes other thanpredation, during the breeding season of N. america-nus (mid summer). Bird populations are not the onlycandidates to be good carrion producers. Certainmammal species, like the Blacktail Prairie Dog (Cy-nomys ludovicianus), have also declined drastically(Miller et al. 1990), and such dense concentrations ofmammals may also support N. americanus popula-tions. A relevant and recent study by Smith et al.(2000) has documented that Nicrophorus adults willuse pre-existing vertebrate burrows for burial of car-casses, and those that do so realize significantlygreater reproductive success as a result. Another doc-umentation of use of vertebrate burrows, specificallybird burrows, by Nicrophorus was made by Wilhelmet al. (2001).

Congener competition

The last hypothesis in Table 1, congener competition,extends from the previous two hypotheses. With bothan increase in vertebrate scavenger pressure (exacer-bated by habitat fragmentation), and a decrease incarrion of the ideal weight size (due to extinction andpopulation declines), the competition between N.americanus and sympatric congeners for sub-opti-mally sized carcasses would be expected to increase.Trumbo (1992) showed that the potential for Nicro-phorus congener competition for carrion increasedwith carcass size. Competitive success of carrion-

feeding flies also increases with carcass size (Scott etal. (1987); l.c.).

The historical geographic range, and presumablythe ecological tolerances, of N. americanus are mostsimilar to its congener Nicrophorus orbicollis. Thissimilarity in ecological niche (geographic range, dielperiodicity, breeding season, etc.), and new phyloge-netic information indicating these species may beeach other’s closest surviving relatives (Szalanski etal. 2000), together suggest that N. americanus and N.orbicollis may be each other’s greatest congenericcompetitors. In surveys for N. americanus, N. orbi-collis is almost always trapped and is usually 10, ormore, times as abundant (e.g., Lomolino and Creigh-ton’s (1996) and Amaral et al. (1997); Carlton andRothwein (1998); Raithel in press). Although N. or-bicollis appears to be less successful in using the larg-est carcasses that N. americanus requires for maxi-mum reproductive success (> 100 g) (Kozol et al.1988; Trumbo 1992), this species could be a formi-dable competitor for smaller and medium sized car-casses.

Another sympatric congener, Nicrophorus mar-ginatus Fabricius, is also often present in traps set forN. americanus (l.c.). Nicrophorus marginatus is onaverage slightly larger (Sikes unpub. data), and insome portions of its range, such as western Nebraska,is more common, than N. orbicollis (Bedick et al.1999). Backlund and Marrone (1997) reported that N.marginatus was the most abundant species collectedduring their surveys for N. americanus in South Da-kota. Interestingly, they also reported that in areas inwhich they caught the most N. americanus, theycaught the least N. marginatus. Nicrophorus margina-tus is well documented as a specialist of open grass-land habitat (Anderson and Peck 1985). If such hab-itat is used more by N. americanus now thanhistorically, perhaps because this species is trackingpopulations of small mammals or gallinaceous birdsthat prefer open habitats, then competition betweenthese two Nicrophorus species may have increased.This relationship has not been investigated. Addition-ally, Kozol et al. (1988) showed that N. marginatusburied larger carcasses than did N. orbicollis. Al-though still probably less successful with the largestcarcasses (> 100 g), N. marginatus could, as a result,be a more significant competitor of N. americanusthan N. orbicollis in areas of sympatry.

Although, N. americanus, because of its largersize, dominates interference competition events -di-rect physical battles at carcasses (Kozol et al. 1988),

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there are data indicating N. orbicollis may dominateexploitative competition events -speed of finding andburying carcasses (Matthews 1995) and thus contrib-ute to the current pressures affecting N. americanus.However, to what degree N. americanus is losing po-tential breeding carcasses (albeit of less than optimalsize), throughout its range, to N. orbicollis and/or N.marginatus remains unstudied.

Burying beetle females that lose battles to securea carcass sometimes oviposit near the carcass, allow-ing some of their larvae to act as brood parasites(Müller et al. 1990; Trumbo 1994). Mixed-speciesbroods are more common on larger carcasses (Trum-bo 1992). Investigations of congener competitionshould be aware of the potential for brood parasitismby either N. orbicollis or N. marginatus within N.americanus broods.

Suggestions for future research

The research reviewed herein provides clues to thetwo related and most important questions that remainunanswered: What parameters predict the currentpresence of Nicrophorus americanus? Also, whatchanges were responsible for the decline of this spe-cies? To answer these questions will require numer-ous corroborative, hypothesis-driven investigations.We suggest the following research as being of thehighest priority:

1. Predicting the current distribution: The distribu-tion of a monophagous herbivore is, in compari-son to that of Nicrophorus americanus, relativelyeasy to predict. The distribution of the host plantwith consideration of competitors, predators andclimatic tolerances of the herbivore is usually suf-ficient to predict where it might occur. However,Nicrophorus americanus is neither monophagousnor herbivorous. Few studies have directly ad-dressed the resource-base of this species. Hollo-way and Schnell’s (1997, 1997) are the only stud-ies that did so - by attempting to quantify thecarrion prey-base and relate these data to the dis-tribution of Nicrophorus americanus. These stud-ies results’ support the conclusion that this speciespersists in areas that have unique vertebrate com-munities but alone are not sufficient to identify N.americanus habitat.

Future investigations in silphid communitystructure should quantify the potential carrionprey-base in addition to, as has been typical, the

carrion-feeding community. If a standardized pro-tocol for collecting and reporting these data couldbe developed, investigators would be able to com-pare habitats according to an index based on theavailable, ideal carrion and the competitive pres-sure for that resource. Such a process could leadto the identification, management, and creation oflandscapes capable of sustaining N. americanuspopulations.

Initially, studies would have to be performedwithin the current Nicrophorus americanus popu-lations to enable accurate description of ‘ideal car-rion’. Such descriptors would include traits suchas average size during the breeding season ofNicrophorus americanus, quantity of carcassesproduced during the breeding season of Nicropho-rus americanus, and habitat affiliation with appro-priate substrate for burial (e.g. nesting gulls usu-ally die on beaches which have unsuitablesubstrates for burial by Nicrophorus americanus).Once we can define quantitatively what constitutesan ideal carrion-producing vertebrate species forNicrophorus americanus we can begin identifyingand ranking suitable candidate species within thehistoric range of Nicrophorus americanus. Such alist, with maps of current and past distributions (asbest as possible), and the research that would gointo quantifying the criteria for inclusion, wouldbe a very valuable step towards predicting thepresence of Nicrophorus americanus.

Of course, the potential prey base is only halfof the needed data. The other part of the equationmust be the intensity of competition for the avail-able, ideal carrion. Areas that see the generationof large quantities of ideal carrion during thebreeding season of Nicrophorus americanus maybe of little value to this species if carcasses are re-moved by vertebrate scavengers before Nicropho-rus americanus can use them. Thus, a protocolshould be developed to allow standardized com-parisons of competitive pressure (broken down byfactors such as vertebrate/invertebrate and vari-ability, among others). Obtaining these data, par-ticularly considering the variation that can occurover time, could be quite challenging, but must beconsidered essential towards understanding thisspecies’ requirements for survival.

2. Explaining the decline: One could argue that oncewe understand the ecological requirements of thisspecies and can predict its persistence, explainingits decline is of little practical importance. For this

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reason we consider understanding the causes ofdecline to be of slightly lower priority than under-standing this species’ current ecological needs.However, if the causal factors of decline persistthroughout the historic range of Nicrophorusamericanus these would necessarily become un-derstood by efforts to describe the potential nicheof Nicrophorus americanus. It is likely, therefore,that by accomplishing the primary goal we will gofar towards explaining the decline of this species.Additionally, efforts to test hypotheses of declinewould likely provide data relevant to predictingthis species’ current, historic, and potential niche.

Summary

It should be clear that several investigations impor-tant to our understanding of the decline of N. ameri-canus remain to be done. Unlike the DDT hypothesis,the effects of artificial lighting can be readily studiedtoday. The pathogen hypothesis is less easily tested.However, conservationists working with populationsof N. americanus for reintroduction or breeding pur-poses should be alert to the possibility of a species-specific pathogen. The evidence against N. america-nus being a habitat specialist of old growth forests,and having declined due to the loss of these forestsand their deeper soils, is strong. The combination ofthe last three hypotheses build the most plausible ex-planation for the decline of this species–a conclusionreached first in Raithel (US Fish and Wildlife Service1991) and subsequently supported and commented onby numerous other authors; (1) reduction of optimallysized carrion, (2) increased vertebrate scavenger com-petition for that carrion, and (3) increased congenercompetition for optimally, and suboptimally sizedcarrion–due, in part, to extinctions or declines of op-timally sized prey populations resulting from habitatchanges, overharvesting, and increased vertebratescavenging and predation. The greater pressure fromvertebrate scavengers may have resulted from com-petitive release after the loss of larger predators (suchas the Gray Wolf [Canis lupus] and the MountainLion [Felis concolor]) and an increase in habitat frag-mentation and edge habitats. Nicrophorus americanusthus may be experiencing greater vertebrate and con-gener competition for a reduced resource base. Pre-sumably, the extant N. americanus populations occurin areas with lower vertebrate and/or congener com-petition and/or a greater resource base, although after

twelve years of study we have yet to confirm this em-pirically throughout the range of N. americanus. Thestory of the decline of the American burying beetleappears to be a tale of changes in vertebrate commu-nity ecology, both of prey and scavenger competitorspecies. Yet, many of the published studies havelooked at vegetation and abiotic correlates rather thanvertebrate ecology.

In summary, after over a decade of research, theseconclusions are not very different than those ofRaithel a decade ago (US Fish and Wildlife Service1991). Since the US Fish and Wildlife Service (1991)recovery plan, new data have been brought to supportthe vertebrate competition (Trumbo and Bloch 2000),and the congener hypothesis (Matthews 1995). Andthere have been other relevant studies, includingChannel and Lomolino (2000) investigation of thegeographic pattern of decline. Yet, until we havelearned more about this species’ ecology and its his-tory, these explanations remain primarily speculative.Of the greatest urgency would be investigations (asdetailed above in Suggestions for future research) thatcontrast multiple portions of the historical center ofN. americanus’ range with the eastern and westernextant populations with regards to habitat fragmentsize, biomass of ideal carrion-resource vertebrates(e.g., Holloway and Schnell’s (1997)), vertebrate pre-dation /scavenger pressure, and congener competi-tion.

Acknowledgements

We thank the following for their comments on earlierversions of this manuscript: Michael Amaral, RobertDunn, Piotr Naskrecki, Carl Schaefer, Sacha Spector,Stephen Trumbo, Michael Wall, and two anonymousreviewers. This work was supported by National Sci-ence Foundation Grant DEB-9981381 to StephenTrumbo.

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