Submitted 28 July 2015Accepted 18 December 2015Published 19 January 2016

Corresponding authorMatthew A Bertonematt_bertonencsuedumatthewbertonegmailcom

Academic editorMarcio Pie

Additional Information andDeclarations can be found onpage 20

DOI 107717peerj1582

Copyright2016 Bertone et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Arthropods of the great indoorscharacterizing diversity inside urban andsuburban homesMatthew A Bertone1 Misha Leong2 Keith M Bayless1 Tara LF Malow3Robert R Dunn45 andMichelle D Trautwein2

1Department of Entomology North Carolina State University Raleigh NC United States of America2California Academy of Sciences San Francisco CA United States of America3North Carolina Museum of Natural Sciences Raleigh NC United States of America4Department of Applied Ecology North Carolina State University Raleigh NC United States of America5Center for Macroecology Evolution and Climate Natural History Museum of DenmarkUniversity of Copenhagen Copenhagen Denmark

ABSTRACTAlthough humans and arthropods have been living and evolving together for all of ourhistory we know very little about the arthropods we share our homes with apart frommajor pest groups Here we surveyed for the first time the complete arthropod faunaof the indoor biome in 50 houses (located in and around Raleigh North CarolinaUSA) We discovered high diversity with a conservative estimate range of 32ndash211morphospecies and 24ndash128 distinct arthropod families per house The majority of thisindoor diversity (73) was made up of true flies (Diptera) spiders (Araneae) beetles(Coleoptera) and wasps and kin (Hymenoptera especially ants Formicidae) Muchof the arthropod diversity within houses did not consist of synanthropic species butinstead included arthropods that were filtered from the surrounding landscape As suchcommon pest species were found less frequently than benign species Some of the mostfrequently found arthropods in houses such as gall midges (Cecidomyiidae) and booklice (Liposcelididae) are unfamiliar to the general public despite their ubiquity Thesefindings present a new understanding of the diversity prevalence and distributionof the arthropods in our daily lives Considering their impact as household pestsdisease vectors generators of allergens and facilitators of the indoor microbiomeadvancing our knowledge of the ecology and evolution of arthropods in homes hasmajor economic and human health implications

Subjects Biodiversity EntomologyKeywords Indoor biome Urban entomology Entomology Arthropod Houses

INTRODUCTIONFor as long as humans have lived in fixed habitations there have been other organismsthat dwell alongside us We share our living spaces with a variety of invited and uninvitedguests spanning the tree of life from large vertebrates (eg pets and livestock) to mi-croorganisms (Martin et al 2015) The most diverse and abundant group of multicellularlife found in homes as well as on Earth more generally is represented by arthropods

How to cite this article Bertone et al (2016) Arthropods of the great indoors characterizing diversity inside urban and suburban homesPeerJ 4e1582 DOI 107717peerj1582

Insects spiders and their relatives have been living and evolving with humans for allof our history It has been proposed that many arthropod species that are now associatedwith human houses were originally cave dwellers (eg bed bugs Cimicidae) (Balviacuten etal 2012) Evidence of arthropod vectors in caves inhabited by prehistoric people ca26000 years ago suggests that pestiferous arthropods such as blood-feeding kissing bugs(Reduviidae Triatominae) lived alongside our ancestors (Arauacutejo et al 2009) Among thefirst examples of cave art is a depiction of a camel cricket (Rhaphidophoridae) (Chopard1928 Belles 1997)

As human society changed over time arthropods successfullymdashand rapidlymdashmadeuse of our bodies and resources for food and shelter Constructed houses animaldomestication agriculture and the ability to store food (such as grains) brought differentarthropod species into the domiciles and daily lives of humans Arthropods are commonfauna in domestic archaeological sites from Egypt (dating as far back at 1353 BCE)Israel and Europe (Switzerland Greenland and the UK) (Nielsen Mahler amp Rasmussen2000 Panagiotakopulu 2001 Panagiotakopulu 2003 Kislev Hartmann amp Galili 2004Panagiotakopulu 2004 Kenward amp Carrott 2006) with some species characteristic ofstored food products and livestock and others representative of local fauna

In contrast to the simple dwellings early humans used modern western houses areperceived of as being an environment largely devoid of animal life However arthropodsthrive in homes as evidenced by todayrsquos multi-billion dollar pest control industry Housestoday host many of the same pest groups found in archeological sites (see lsquoResultsrsquo)yet todayrsquos arthropod communities also reflect aspects of societyrsquos modernization Forexample with the advent of indoor plumbing dung beetles (Scarabaeidae) are lessprevalent indoors (as shown in this study) but drain-dwelling moth flies (Psychodidae)are likely more so Also as human society became more globalized through travel andtrade arthropod species that are closely associated with humans and their homes suchas the house fly (Musca domestica L Legner amp McCoy 1966) German cockroach (Blattellagermanica L) and fruit fly (or vinegar fly Drosophila melanogaster Meigen Keller 2007)obtained worldwide distributions and in some cases even lack wild populations (eg theGerman cockroach Roth 1985 Booth et al 2010) The influence of human society andour changing domiciles on the evolution of specific arthropod lineages is evident

Research on indoor arthropod communities has focused almost exclusively on pestswith a particular emphasis on those of medical and economic importance such as cock-roaches termites bed bugs fleas and mosquitoes (Committee on Urban Pest Managementet al 1980 Robinson 2005) Unlike the species that threaten or bother us very little isknown about the myriad other arthropod species many of them inconspicuous (andeven unnoticed) that live with humans The true interactions between these other speciesand humansmdashbe it beneficial neutral or negativemdashremain largely unknown as doestheir prevalence and distribution In fact a comprehensive survey of arthropod life incontemporary human houses has never before been carried out

A systematic sampling of the complete arthropod fauna in the interior of homes and anunderstanding of the role that interior microhabitats play in determining the assemblageof arthropod communities are the first steps toward revealing ecological dynamics in a

Bertone et al (2016) PeerJ DOI 107717peerj1582 223

vastly understudied system (Baz amp Monserrat 1999 Dunn et al 2013) What are the mostprevalent arthropod groups found in houses and how common are they among homesand rooms Here we explored the composition of overall arthropod diversity includingboth pest and non-pest species in human dwellings Through surveying 50 free-standinghouses located in the North Carolina Piedmont region we identified and characterizedthe overall diversity of arthropods found within these homes

MATERIALS amp METHODSWe solicited volunteers owning or renting free-standing homes in Raleigh and neigh-boring areas of North Carolina USA The study area is located in the Piedmont of thestate and characterized by red clay soils and deciduouspine forests (with meadowsand aquaticsemi-aquatic systems interspersed) among various urban and suburbandevelopment (Fig 1) We randomly selected 50 homesvolunteers to visit from amongparticipants who filled out an online questionnaire about the characteristics of theirhousehold and behavior of its residents All homes included in the study were withina 30 mile radius of Raleighrsquos center (357719N 786389W) Each home was visitedonce between May and October 2012 Upon arrival volunteers were informed of theprocedures and process for sampling arthropods and asked to sign a consent form(Supplemental Information 1)

General arthropod samplingWe (trained entomologists) performed a visual inspection of each room and collectedspecimens by hand using forceps aspirators and entomological nets Only visiblesurfaces including those accessible under and behind furniture around baseboardsceilings and on shelves and other surfaces were sampled We collected all arthropods orputative arthropods including those from spider webs both living and dead arthropodswere collected in this manner into vials containing 95 ethanol We did not collectall specimens of a given arthropod species We designated each distinct room or areaand labeled its vial with the room name (as best identified) floor type and number ofwindows and doors to the outside of the house doors between rooms were not quantifiedWe identified floor types as wood (including laminates hardwoods and other wood-likesurfaces) linoleum (tiles or otherwise) tile (stone concrete or otherwise not includinglinoleum) or carpet The presence of small or large rugs on other surfaces was notedas well Typical room categories included kitchens bedrooms (sometimes specified asofficesdens because of their lack of running water but not receiving the same amountof traffic as common areas) bathrooms laundryutility rooms (denoted when a washerand dryer were present) and common areas Common areas consisted of large openareas that were not easily categorized usually including dining rooms living rooms frontrooms hallways etc Closets were sampled and included with the room in which theyopened When a room was present on a floor other than the firstmain floor house levelwas recorded (eg lsquolsquo2nd Floor Bathroomrsquorsquo) All rooms inside the house were sampledin the manner described above except for attics and crawl spaces which were sampledless thoroughly only the entrance of each was sampled within a 2 m radius The limited

Bertone et al (2016) PeerJ DOI 107717peerj1582 323

Figure 1 Map of study sites Fifty homes (denoted by stars) were selected in and around the RaleighNorth Carolina area Raleigh is within Wake County highlighted in red on the state map below thoughsome samples fell within adjacent counties

sampling method for these areas was deemed necessary for the safety of those collectingthe specimens (ie to avoid high summer temperatures in attics and confined areas incrawl spaces) Screened porches decks garages detached shedsstructures and closetsaccessible only from the outside were not sampled

Dust mitesWe sampled dust mites from the middle of the master bedroom floor regardless offloor type in a 05 m2 area To collect mites we used a vacuum that was adapted touse specimen cups modified with a screen bottom composed of mesh with 00055 inch(01397 mm) openings small enough to allow air to pass through but not mites We

Bertone et al (2016) PeerJ DOI 107717peerj1582 423

stored all samples in 95 ethanol until they were sorted and quantified Because of timeand specimen handling constraints only five individuals from five randomly-selectedsamples were identified

Identification and classificationWe identified all specimens to family level except when specimens were badly damaged orrequired additional methods for identification (eg slide mounting of mites and othertaxa) We further determined genera and species when possible but many specimenscould not be identified to such a level for several reasons including but not limited tobeing damaged being an unidentifiable sex (eg female Sciaridae) or an unidentifiablelife stage (eg larvae) or being a group that is understudied or lacking good diagnostickeys As such our approach produced a very conservative list of morphotaxa for eachroom in the house and hereafter we call these morphospecies this type of characterizationhas been found to be effective in comparing species richness and turnover between sites(Oliver amp Beattie 2002) The taxonomic identity of morphospecies was not comparedbetween rooms within homes due to limitations on time space (storage of voucherspecimens) and diagnostic expertise thus the true number of morphospecies per houseand among all houses was not definitively determined Thus a conservative (or assumedminimum) estimate of morphospecies richness per house was created by taking themaximum number of morphospecies from the room containing the highest number ofmorphospecies for each family and summing the total This is in contrast to a maximumestimate of morphospecies richness which was the total sum of all morphospeciesfrom all rooms within a house this maximum corresponds to the case in which no tworooms held the same morphospecies We assume the true diversity falls between ourminimum and maximum estimates All voucher specimens are housed in vials of ethanolin the laboratory of RRD (Department of Biological Sciences NCSU) for use in furtherecological genetic and microbiological studies Specimens will be deposited in the insectmuseum at NCSU (Department of Entomology) when permanently housed

AnalysesWe classified rooms into 6 categories based on their similarities of features and use atticsbasements (including finished and unfinished basements and crawl spaces) bathrooms(including bathrooms and laundry rooms) bedrooms (including bedrooms offices andlibraries) common rooms (including living rooms dining rooms and attached hallways)and kitchens (including kitchens and pantries) rooms not conforming to one of thecategories were classified as lsquolsquootherrsquorsquo and were excluded from Table 1 We estimateddiversity of families based on the complete list of families acquired over each sampledhouse using the Chao2 Estimator with 1000 randomization runs in EstimateS (Colwell2013) We compared total dust mite abundance in each sample with the floor type onwhich it was collected Some samples were collected on carpet while others were on baresurfaces Because the data were not normally distributed we analyzed the differencesbetween samples with different floor types using a KruskalndashWallis test All analyses weredone in R 312 (R Core Team 2015)

Bertone et al (2016) PeerJ DOI 107717peerj1582 523

Table 1 List of arthropods found during the study present in at least 10 (n = 5) of homes Table includes the percentage of homes rooms overall and six specificroom types (attics basements bathrooms bedrooms common areas and kitchens) where a taxon was collected One hundred twenty-eight additional families were col-lected but were found in less than 10 (n = 5) of homes For the full table containing all taxa (including genera and species that were identified) see Table S1 All namesare based on current taxonomy except for mites where lsquolsquoAcarirsquorsquo is used as a general order despite modern classifications that consider the group a subclass with numerousorders (Krantz amp Walter 2009) sl= sensu lato ie lsquolsquobroad sensersquorsquo

Class Order Family Common name Homes(n= 50)

Rooms(n= 554)

Attic(n= 38)

Basement(n= 54)

Bath(n= 146)

Bed(n= 160)

Common(n= 97)

Kitchen(n= 50)

Entognatha (non-insect hexapods) 88 229 53 259 158 219 371 260Collembola (springtails) 88 229 53 259 158 219 371 260

Entomobryidae slender springtails 78 191 53 204 151 169 289 240Tomoceridae elongate springtails 26 36 ndash 19 07 38 93 40

Insecta (true insects) 100 949 789 963 911 981 979 1000Archaeognatha (jumping bristletails) 18 25 ndash 19 27 19 52 20

Machilidae jumping bristletails 14 20 ndash 19 14 13 52 20Zygentoma (silverfish) 68 213 211 37 151 231 402 160

Lepismatidae silverfish amp firebrats 68 213 211 37 151 231 402 160Dermaptera (earwigs) 50 76 ndash 167 41 63 144 60

Anisolabididae earwigs 26 36 ndash 93 27 25 62 20Forficulidae earwigs 24 34 ndash 74 14 31 62 40

Orthoptera (grasshoppers crickets amp katydids) 76 177 26 537 75 113 299 140Gryllidae crickets 30 36 ndash 56 21 38 82 ndashMyrmecophilidae ant-loving crickets 10 09 ndash ndash ndash ndash 21 60Rhaphidophoridae camel amp cave crickets 58 128 ndash 500 55 69 196 60

Blattodea (cockroaches) 82 255 184 333 144 263 433 180Blattidae cockroaches 74 229 158 333 123 225 402 160Ectobiidae cockroaches 34 43 26 56 21 38 103 20

Isoptera (termites) 28 49 ndash 37 14 44 124 60Rhinotermitidae subterranean termites 28 49 ndash 37 14 44 124 60

Hemiptera (true bugs) 98 363 79 278 185 369 680 580Anthocoridae minute pirate bugs 42 60 ndash ndash 27 56 165 80Aphididae aphids 56 76 26 74 14 63 155 200Cicadellidae leafhoppers 82 162 ndash 56 89 138 371 300Coreidae leaf-footed bugs 12 11 26 ndash ndash 13 31 ndashCydnidae burrowing bugs 28 29 26 37 14 19 82 ndashDelphacidae delphacid planthoppers 12 14 ndash 19 14 06 31 ndashLygaeidae seed bugs 10 14 ndash ndash 07 13 41 ndashMiridae plant bugs 44 65 ndash ndash 21 56 196 80

(continued on next page)

Bertone

etal(2016)PeerJDOI107717peerj1582

623

Table 1 (continued)

Class Order Family Common name Homes(n= 50)

Rooms(n= 554)

Attic(n= 38)

Basement(n= 54)

Bath(n= 146)

Bed(n= 160)

Common(n= 97)

Kitchen(n= 50)

Pentatomidae stink bugs 22 25 53 ndash ndash 31 52 40Psyllidae sl jumping plant lice 10 09 ndash ndash 07 ndash 31 20Reduviidae assassin bugs 28 34 ndash 37 ndash 19 113 40Rhyparochromidae dirt-colored seed bugs 30 38 ndash 37 41 19 93 20Tingidae lace bugs 16 16 ndash 19 14 13 41 ndash

Psocodea (lice) 98 431 368 241 315 506 608 460Ectopsocidae bark lice 16 20 ndash ndash ndash 25 52 40Lepidopsocidae scaly-winged bark lice 24 43 26 ndash 07 56 134 ndashLiposcelididae book lice 98 374 342 167 281 444 526 380

Thysanoptera (thrips) 50 70 26 56 27 44 196 80Phlaeothripidae tube-tailed thrips 14 14 ndash 19 07 06 52 ndashThripidae common thrips 32 42 26 ndash 21 25 113 60

Hymenoptera (wasps ants amp bees) 100 697 500 648 507 788 856 840Bethylidae bethylid wasps 28 38 ndash 19 07 25 144 20Braconidae braconid wasps 52 76 ndash ndash 41 88 196 60Ceraphronidae ceraphronid wasps 14 14 ndash 19 ndash ndash 72 ndashChalcididae chalcidid wasps 14 14 ndash ndash 07 19 41 ndashDiapriidae diapriid wasps 26 25 ndash 56 ndash 13 82 20Encyrtidae encyrtid wasps 12 14 ndash ndash ndash 19 41 ndashEulophidae eulophid wasps 70 170 ndash 74 130 169 309 220Formicidae ants 100 619 474 574 418 663 814 820Halictidae sweat bees 10 09 26 19 07 ndash ndash 40Ichneumonidae ichneumon wasps 38 45 26 56 14 44 93 40Mymaridae fairyflies 26 23 ndash ndash 07 ndash 113 20Platygastridae sl platygastrid wasps 58 83 ndash ndash 62 56 278 20Pompilidae spider wasps 34 65 26 74 27 56 175 ndashPteromalidae pteromalid wasps 42 49 ndash ndash 21 38 103 160Sphecidae sl thread-waisted wasps 26 32 26 19 27 38 62 ndashVespidae paper wasps amp hornets 14 16 53 19 - 19 31 ndash

Neuroptera (lacewings antlions etc) 56 69 ndash 37 27 44 206 100Chrysopidae green lacewings 34 36 ndash 19 14 25 113 40Coniopterygidae dustywings 16 14 ndash ndash 07 13 41 20Hemerobiidae brown lacewings 18 18 ndash ndash ndash ndash 72 60

Coleoptera (beetles) 100 720 447 648 541 844 918 720Aderidae ant-like leaf beetles 22 25 ndash ndash 07 31 52 60Anobiidae death watch beetles 60 121 ndash 74 55 106 309 140

(continued on next page)

Bertone

etal(2016)PeerJDOI107717peerj1582

723

Table 1 (continued)

Class Order Family Common name Homes(n= 50)

Rooms(n= 554)

Attic(n= 38)

Basement(n= 54)

Bath(n= 146)

Bed(n= 160)

Common(n= 97)

Kitchen(n= 50)

Anthicidae ant-like flower beetles 18 23 26 ndash 07 19 72 ndashCarabidae ground beetles 66 99 79 333 41 69 144 20Cerambycidae longhorned beetles 16 16 ndash ndash 07 31 31 ndashChrysomelidae leaf beetles 46 60 ndash ndash 14 81 175 20Cleridae checkered beetles 18 18 ndash ndash 14 31 31 ndashCoccinellidae ladybugs 52 78 53 19 07 88 227 40Cryptophagidae silken fungus beetles 26 32 ndash ndash ndash 25 124 40Curculionidae weevils bark beetles 82 157 26 185 96 163 340 60Dermestidae carpet beetles 100 570 263 222 445 713 825 580Elateridae click beetles 74 146 53 130 55 125 392 80Histeridae clown beetles 10 09 ndash 19 07 06 21 ndashLampyridae fireflies 20 22 26 19 ndash 13 62 40Latridiidae minute brown scavenger

beetles38 63 ndash 19 14 56 165 120

Melyridae soft-winged flower beetles 20 29 ndash 19 27 31 52 20Mordellidae tumbling flower beetles 24 36 26 37 07 31 82 40Mycetophagidae hairy fungus beetles 20 18 26 ndash ndash 25 41 20Nitidulidae sap beetles 24 31 ndash 37 ndash 25 103 20Phalacridae shining flower beetles 12 13 ndash 19 ndash 06 52 ndashPtilodactylidae ptilodactylid beetles 30 49 26 37 21 56 93 60Scarabaeidae scarab beetles 52 94 53 130 27 81 206 100Scraptiidae false flower beetles 20 20 ndash ndash 07 19 62 20Silvanidae flat bark beetles 46 65 ndash 93 21 50 175 40Staphylinidae rove beetles 54 72 ndash 74 48 50 175 60Tenebrionidae darkling beetles 62 112 53 167 48 113 247 20Throscidae false metallic wood boring

beetles22 27 ndash 19 07 19 93 20

Trogossitidae bark gnawing beetles 16 14 ndash ndash 07 06 62 ndashZopheridae ironclad beetles 16 14 ndash ndash ndash 25 10 60

Lepidoptera (moths amp butterflies) 92 287 ndash 167 116 338 567 380Geometridae geometrid moths 12 16 ndash 19 07 19 21 20Noctuidae owlet moths 44 58 ndash 37 41 50 124 60Pyralidae pyralid moths 62 110 ndash 37 48 125 216 220Tineidae clothes moths 60 88 ndash ndash 55 94 196 100Tortricidae leafroller moths 10 11 ndash ndash 07 06 41 ndash

(continued on next page)

Bertone

etal(2016)PeerJDOI107717peerj1582

823

Table 1 (continued)

Class Order Family Common name Homes(n= 50)

Rooms(n= 554)

Attic(n= 38)

Basement(n= 54)

Bath(n= 146)

Bed(n= 160)

Common(n= 97)

Kitchen(n= 50)

Trichoptera (caddisflies) 12 11 ndash ndash 07 13 31 ndashSiphonaptera (fleas) 10 14 ndash ndash 27 13 10 20

Pulicidae cat dog amp human fleas 10 14 ndash ndash 27 13 10 20Diptera (true flies) 100 718 184 500 664 856 856 800

Agromyzidae leafminer flies 12 11 ndash ndash 07 06 31 20Anisopodidae wood gnats 10 09 ndash ndash ndash 06 31 20Anthomyiidae root maggot flies 10 09 ndash ndash ndash 13 10 40Bibionidae march flies lovebugs 26 27 ndash ndash 07 38 72 20Calliphoridae blow flies 48 81 ndash 56 27 75 237 60Cecidomyiidae gall midges 100 361 105 167 301 338 639 460Ceratopogonidae biting midges 54 76 ndash ndash 34 88 186 100Chaoboridae phantom midges 14 34 ndash ndash 34 19 82 60Chironomidae non-biting midges 80 170 ndash 37 89 138 423 300Chloropidae frit flies 28 43 ndash ndash 34 31 103 80Culicidae mosquitoes 82 190 ndash 56 75 244 412 220Dolichopodidae longlegged flies 44 49 ndash 37 27 44 124 40Drosophilidae fruit flies vinegar flies 66 137 ndash 56 48 156 299 220Empididae sl dance flies 16 18 ndash 19 07 13 62 ndashEphydridae shore flies 14 14 ndash ndash 14 ndash 62 ndashFanniidae lesser house flies 10 11 ndash 19 07 06 10 40Lauxaniidae lauxaniid flies 16 16 ndash ndash 07 13 62 ndashMilichiidae freeloader flies 14 16 ndash ndash 07 19 41 ndashMuscidae house amp stable flies 44 63 26 56 14 56 165 40Mycetophilidae sl fungus gnats 68 162 ndash 93 82 206 371 60Phoridae scuttle flies 82 173 ndash 204 62 169 392 180Psychodidae moth flies 74 188 ndash 93 144 181 412 140Sarcophagidae flesh flies 38 51 ndash ndash 27 44 124 60Scatopsidae minute black scavenger flies 50 69 ndash 19 55 44 165 100Sciaridae dark-winged fungus gnats 96 421 ndash 222 356 494 649 420Sphaeroceridae lesser dung flies 28 34 26 111 21 25 52 ndashStratiomyidae soldier flies 22 23 ndash 19 07 06 82 20Tachinidae tachinid flies 18 16 ndash ndash ndash 19 52 20Tipulidae sl crane flies 74 159 26 74 110 169 320 180Trichoceridae winter crane flies 20 23 ndash 19 21 19 62 ndash

(continued on next page)

Bertone

etal(2016)PeerJDOI107717peerj1582

923

Table 1 (continued)

Class Order Family Common name Homes(n= 50)

Rooms(n= 554)

Attic(n= 38)

Basement(n= 54)

Bath(n= 146)

Bed(n= 160)

Common(n= 97)

Kitchen(n= 50)

Arachnida (arachnids) 100 796 474 944 685 781 969 900Araneae (spiders) 100 785 474 926 685 756 969 880

Agelenidae funnel weavers grassspiders

46 83 26 204 21 69 165 60

Anyphaenidae ghost spiders 30 43 ndash 19 07 56 113 40Araneidae orb weavers 18 22 ndash 19 14 13 62 20Clubionidae sac spiders 10 09 ndash ndash ndash ndash 41 20Corinnidae antmimics ground spiders 38 60 53 93 14 69 113 40Gnaphosidae ground spiders 48 81 ndash 56 34 100 206 20Linyphiidae sheetweb amp dwarf spiders 22 29 ndash 37 ndash 13 103 20Lycosidae wolf spiders 40 58 26 56 21 25 165 80Oecobiidae wall spiders 28 88 26 ndash 62 100 186 80Oonopidae goblin spiders 16 32 53 ndash 21 38 62 20Pholcidae cellar spiders 84 280 79 389 192 181 567 320Salticidae jumping spiders 50 83 26 37 27 75 227 60Scytodidae spitting spiders 16 27 ndash 19 34 25 41 20Theridiidae cobweb spiders 100 653 395 778 555 613 876 700Thomisidae crab spiders 32 34 26 19 ndash 44 93 20

lsquolsquoAcarirsquorsquo (mites) 76 186 53 463 48 175 361 100Galumnidae armored mites 12 11 ndash 19 ndash 06 41 ndashIxodidae hard ticks 18 20 ndash ndash 07 19 72 ndashUnID Oribatida armored mites 46 60 ndash 222 14 38 124 20Pyroglyphidae dust mites 76 NA NA NA NA NA NA NA

Opiliones (harvestmen amp daddy-longlegs) 16 23 26 37 07 25 52 -Pseudoscorpionida (pseudoscorpions) 20 27 ndash 37 07 06 103 20

Chilopoda (centipedes) 42 92 ndash 167 41 94 165 100Lithobiomorpha (stone centipedes) 18 18 ndash 19 ndash 19 52 20

Lithobiidae stone centipedes 14 13 ndash 19 ndash 19 21 20Scolopendromorpha (tropical centipedes) 12 22 ndash 56 07 19 52 ndash

Scolopendridae tropical centipedes 12 22 ndash 56 07 19 52 ndashScutigeromorpha (house centipedes) 32 69 ndash 130 34 69 103 100

Scutigeridae house centipedes 32 69 ndash 130 34 69 103 100

Diplopoda (millipedes) 82 211 53 630 62 150 381 160Callipodida (crested millipedes) 10 18 ndash 56 ndash 25 31 ndash

Abacionidae crested millipedes 10 18 ndash 56 ndash 25 31 ndash(continued on next page)

Bertone

etal(2016)PeerJDOI107717peerj1582

1023

Table 1 (continued)

Class Order Family Common name Homes(n= 50)

Rooms(n= 554)

Attic(n= 38)

Basement(n= 54)

Bath(n= 146)

Bed(n= 160)

Common(n= 97)

Kitchen(n= 50)

Julida (julid millipedes) 42 47 ndash 185 21 25 93 ndashJulidae millipedes 38 38 ndash 111 21 25 82 ndash

Polydesmida (flat-backedmillipedes) 72 177 53 574 48 131 299 140Paradoxosomatidae greenhouse millipedes 58 126 26 426 27 94 227 100Polydesmidae flat-backed millipedes 26 43 ndash 167 14 13 82 40

Spirobolida (round-backedmillipedes) 20 23 ndash 148 07 ndash 31 20Spirobolidae round-backed millipedes 18 22 ndash 148 07 ndash 21 20

Malacostraca (crustaceans) 86 238 53 574 144 200 340 220Isopoda (isopods) 84 236 53 574 144 200 340 200

Armadillidiidae pillbugs amp roly polies 78 220 53 481 137 188 330 200Porcellionidae woodlice amp sowbugs 20 42 ndash 148 14 38 52 40

Bertone

etal(2016)PeerJDOI107717peerj1582

1123

Figure 2 Estimated diversity of families The mean along with 95 lower and upper confidence in-tervals was calculated based on the complete list of families acquired over each sampled house using theChao2 Estimator with 1000 randomization runs in EstimateS (Colwell 2013)

RESULTSOverall metricsHouses in the study ranged from 840 to 4833 square feet in area (mean= 2072median= 1720) and were from seven to 94 years old (mean= 4135 median= 305)During the course of sampling 554 rooms in the 50 homes over 10000 specimens werecollected and identified These specimens represented all four subphyla (ChelicerataMyriapoda lsquolsquoCrustacearsquorsquo and Hexapoda) as well as six classes 34 orders and 304 familiesof arthropods (Table 1 and Table S1) While we cannot determine the exact numberof morphospecies that were collected there were at least 579 morphospecies based onour most conservative estimates (calculated by summing the maximum number ofmorphospecies for each family ever found in a single room)

We collected 24ndash128 families from each house resulting in an average of 6184 (sd=2324) distinct arthropod families per house and a total gamma diversity (across houses)of 304 families (Fig 2) One hundred and forty-nine (149) families were rare collectedfrom fewer than 10 of homes 66 of which were found in just a single home Thenumber of families collected in a home was correlated with house size (r2 = 03 p=lt0001) Conservative species estimates by home ranged from 32 to 211 with an average of9314 (sd= 4234) morphospecies per house (Fig 3) Considering that our conservativespecies estimate assumes that rooms with the greatest number of morphospecies by familyincluded all species from other rooms (which is almost certainly untrue) this number islikely much lower than the true number of species per house (Fig 3)

Bertone et al (2016) PeerJ DOI 107717peerj1582 1223

Figure 3 Number of species by house (in ascending rank order of house size) The number of species collected by house is represented by themiddle bar The bottom limit is the minimumconservative estimate of morphospecies by house which was calculated by taking the maximum num-ber of morphospecies from the room containing the highest number of morphospecies for each family and summing the total The upper limit isthe maximum possible of morphospecies within a house with the assumption that each set of morphospecies within each room were unique fromother rooms Houses furthest to the left are the smallest in terms of square footage and those furthest to the right are the largest Houses ranged insize from 840 to 4833 square feet

Taxon specific observationsWhile overall diversity was high 12 frequently found families were identified in atleast 80 of homes (Fig 4) Only four families were identified from 100 of housessampled cobweb spiders (Theridiidae) carpet beetles (Dermestidae) gall midge flies(Cecidomyiidae) and ants (Formicidae) Book lice (Liposcelididae) and dark-wingedfungus gnats (Sciaridae) were found in 98 and 96 of homes respectively Nearly half

Bertone et al (2016) PeerJ DOI 107717peerj1582 1323

Figure 4 Photographic representatives of the most frequently collected arthropod families Twelve(12) families were represented in at least 80 of homes For each family we present the common nameand percentage of homes it was found in followed in parentheses by the scientific family name and specieslevel identification when possible (A) cobweb spiders 100 (Theridiidae shown here Parasteatoda tepi-dariorum (Koch)) (B) carpet beetles 100 (Dermestidae shown here Anthrenus larvae) (C) gall midges100 (Cecidomyiidae) (D) ants (continued on next page )

Bertone et al (2016) PeerJ DOI 107717peerj1582 1423

Figure 4 ( continued)100 (Formicidae shown hereMonomorium minimum (Buckley)) (E) book lice 98 (Liposcelididae)(F) dark-winged fungus gnats 96 (Sciaridae) (G) cellar spiders 84 (Pholcidae shown here Pholcussp) (H) weevils 82 (Curculionidae shown here Sitophilus zeamais (Motschulsky)) (I) mosquitoes82 (Culicidae shown here Aedes albopictus (Skuse)) (J) scuttle flies 82 (Phoridae shown hereDohrniphora incisuralis (Loew)) (K) leafhoppers 82 (Cicadellidae shown here Sibovia sp) (L)non-biting midges 80 (Chironomidae) All photos by MAB

of all families (five of 12) found in over 80 of homes were true flies (Diptera) fungusgnats (Sciaridae) mosquitoes (Culicidae) scuttle flies (Phoridae) non-biting midges(Chironomidae) and gall midges (Cecidomyiidae)

Typical household pests were found in a minority of the homes such as Germancockroaches (Blattella germanica 6 of houses) subterranean termites (Rhinotermitidae28 of houses) and fleas (Pulicidae 10 of houses) bed bugs (Cimex lectularius Lin-naeus) were not found during the study Larger cockroaches (Blattidae) such as smokybrown (Periplaneta fuliginosa (Serville)) and American cockroaches (Periplaneta amer-icana (Linnaeus)) were found in the majority of houses (74) However the Americancockroach (which is the only of the two considered a true pest) was only recovered fromthree homes smoky brown cockroaches made up the vast majority of large cockroachescollected All pest species were less common than other more inconspicuous arthropodssuch as pillbugs (Armadillidiidae 78) and springtails (Entomobryidae 78)

In addition to those listed above many of the same pests we recovered were alsofound in archaeological sites (Nielsen Mahler amp Rasmussen 2000 Panagiotakopulu2001 Panagiotakopulu 2003 Kislev Hartmann amp Galili 2004 Panagiotakopulu 2004Kenward amp Carrott 2006) These included grain weevils (Curculionidae SitophilusSchoenherr) carpet beetles (Dermestidae Anthrenus) grain beetles (Silvanidae Oryza-ephilus Ganglbauer) cigarette and drugstore beetles (Anobiidae Lasioderma Stephens ampStegobiumMotschulsky respectively) house flies (MuscidaeMusca domestica) and lesserhouse flies (Fanniidae Fannia Robineau-Desvoidy)

Arthropod distribution within the homeArthropods were found on every level of the home and in all room types Only 5 rooms(non-attics) had no arthropod specimens collected (four bathrooms one bedroom)Six arthropod orders dominated houses comprising 81 of the diversity in an averageroom Diptera (true flies 23) Coleoptera (beetles 19) Araneae (spiders 16)Hymenoptera (predominantly ants 15) Psocodea (book lice 4) and Hemiptera(true bugs 4) (Fig 5) Eight additional orders made up another 15 of the diversity(Blattodea Collembola Lepidoptera Isopoda Zygentoma Polydesmida Orthoptera andAcari) while all remaining orders comprised a total of 4 of the overall diversity (Fig 5)The percentage of rooms in which an arthropod was collected varied among taxa as didtheir presence in rooms of different types (Table 1)

Dust mite samplingDust mite samples contained from 0 to 421 total specimens with an average of 3812 (sd= 715) dust mites were found in 76 of the homes sampled (Table 1) Significantly

Bertone et al (2016) PeerJ DOI 107717peerj1582 1523

Figure 5 Proportional diversity of arthropod orders across all rooms Average morphospecies compo-sition calculated across all room types All photos by MAB

more mites were collected from carpeted surfaces than hard surfaces (eg wood floors)(KruskalndashWallis test χ2

= 10692 p= 0001) Of those identified from the subset all wereDermatophagoides sp (Pyroglyphidae)

DISCUSSIONAs household pests and disease vectors the indoor arthropods in our daily lives have hada substantial impact on human society both historically and today Although extensiveresearch has been done on a small number of arthropod pest species the data presentedherein represent the first comprehensive survey of the arthropod diversity collectedfrom urban and suburban houses In the absence of similar studies that could providebaseline data for comparison our results are surprising both in terms of the prevalenceof arthropods (virtually every room was occupied) and in terms of their diversity

The diversity of arthropods found indoors extends far beyond commonly recognizedspecies We found that an individual house may have hundreds of arthropod specieswithin it with each house on average containing 62 families and a minimum estimateof 93 morphospecies The true diversity among these 50 homes is undoubtedly much

Bertone et al (2016) PeerJ DOI 107717peerj1582 1623

higher due to limitations of the minimum estimate (it assumes no species turnoverbetween rooms) the presence of cryptic species and our sampling method that excludedareas behind walls under heavy furniture and in drawers and cabinets all of whichundoubtedly serve as potential refuges for additional arthropods While sampling 50homes did lead to a decrease in the estimated diversity of families clearly there are stillmany other families and morphospecies that are yet to be recovered and characterizedfrom homes (Fig 2)

We found that four groups of arthropods dominate the average room flies (23)beetles (19) spiders (16) and hymenoptera (predominantly ants 15) (Fig 5)Overall there are more types of flies associated with human homes than any othergroup of animals Some flies have evolved close associations with humans while others(Chironomidae and Cecidomyiidae) may arrive in houses as part of lsquoair planktonrsquo theirpresence indoors is more a reflection of their abundance outdoors than of the ecologyinside homes Despite their prevalence flies represent only a small proportion of taxon-focused studies in the urban landscape (McIntyre 2000) Recent studies have revealed newinformation on flies in urban landscapes including 30 new scuttle fly species identifiedfrom urban Los Angeles (California USA) indicating that the true diversity of these fliesand likely many other small fly groups in human-developed areas is underestimated(Grimaldi et al 2015 Hartop Brown amp Disney 2015)

Book lice (Psocodea Liposcelididae) were found to be among the most ubiquitousindoor arthropods (found in 49 of 50 houses) Book lice are close relatives of parasitic liceand have a long evolutionary history of living among other places in close associationwith birds mammals and their nests (including those of primates Grimaldi amp Engel2005) As stored grain pests fungus feeders and scavengers book lice thrive in indoorenvironments Liposcelis bostrychophila Badonnel for example is a globally-distributedanthropophilic species whose widespread success and resistance to control measures isin part due to its parthenogenesis ability to disperse through air wide diversity of dietand resistance to starvation (Diaz-Montano et al 2014) Book lice have become morecommon in houses in the United Kingdom over time (recovered from 14 of housessampled in 1987 versus 30 in 1997 Turner amp Bishop 1998) and are more prevalentin areas of high humidity in houses in Spain (such as kitchens and bathrooms Bazamp Monserrat 1999) However perhaps due to North Carolinarsquos humid climate or oursampling methods we found book lice distributed throughout houses

Dust mites were found in the majority of homes (76) Previous studies have founddust mites in 30ndash100 of sampled homes across the US (Arlian et al 1992) Humanassociation with dust mites may have been established with the origins of dense humansettlements dust mites likely shifted from the nests of synanthropic birds or rodents tohuman houses (Klimov amp OrsquoConnor 2013) To control dust mite populations it is oftenrecommended to remove carpets because they provide protection thermoinsulationhigher humidity and trap the food on which these mites feed (Colloff 1998) As expectedwe found much higher dust mite abundance on carpeted surfaces consistent withprevious research Yet paradoxically the house that had the single highest abundance ofdust mites within our study had a wood floor Humidity levels and vacuuming frequency

Bertone et al (2016) PeerJ DOI 107717peerj1582 1723

although unknown for this house may explain the discrepancy Characteristics ofdifferent wood floors such as age and quality of build could also affect mite abundancesince gaps between boards can provide habitat for mite populations

Because previous studies of indoor arthropods have largely focused on pest groups ofeconomic and human health importance (eg Runstrom amp Bennett 1990 Colloff 1998How amp Lee 2010 Crissman et al 2010) we expected common pests to be among the mostfrequently found groups of arthropods in the homes In fact we found a relative dearthof typical household pests The only exception to this was the prevalence of the smokybrown cockroach a species that is not truly considered pestiferous because it does notgenerally develop pest-level populations in homes due to its need for high humidity andmoisture (Robinson 2005) It may be that we collected more specimens of this speciesdue to their intolerance and ultimate death within the homes While the lack of many pestspecies could be an artifact of the sampling design (sampling for species occurrence ratherthan abundance as well as sampling in free-standing homes rather than other forms ofhuman habitation such as apartments townhouses etc) it appears that the vast majorityof arthropods that live among us cause no direct harm Unfortunately many insects andarthropods we collected are considered pests based solely on their presence in the home(ie nuisance invaders Hahn amp Ascerno 1991 Cranshaw 2011) despite having no directimpact on people or their possessions

Many arthropods we identified from houses were unexpectedmdasheither in terms of thefrequency with which they were found or because they are rarely found outdoors muchless indoors Gall midges (Cecidomyiidae) although found in every house sampled werenot even mentioned among the over 2000 species listed in a recent compilation of urbaninsects and arachnids (Robinson 2005) Leafhoppers (Cicadellidae) as plant feeders arenot associated with the indoor biome (Robinson 2005) yet were among the groups mostfrequently found in houses Moths and butterflies (Lepidoptera) on the other handwere collected infrequently making up only 2 of the average diversity in a room thisis disproportionate to their known overall diversity (the order comprising over 10 ofdescribed insect species Heppner 2008) Although ants (Formicidae) were expected andfound in 100 of houses further identification at the genus and species level revealed taxathat are not typically thought to occur in homes Camel crickets (Rhaphidophoridae) areknown basement dwellers in the Southeastern US but our sampling confirmed previousreports that an invasive species Diestrammena asynamora (Adelung) predominates overnative species (Ceuthophilus spp) (Epps et al 2014) Other unexpected finds were ant-loving crickets (Myrmecophilidae) the smallest orthopterans (Whitman 2008) whichwere found in homes with ant infestations beetles from the relatively rare suborderArchostemata (families Cupedidae and Micromalthidae) and a larval beaded lacewing(Berothidae) a rarely seen neuropteran known to live within termite nests where theyparalyze termites with an airborne chemical before feeding on them (Johnson amp Hagen1981)

Of the arthropods we found that live out a portion of their life cycle in human housesthere is a broad diversity of trophic levels and life histories represented Apart from afew herbivorous arthropods associated with houseplants or those inadvertently living

Bertone et al (2016) PeerJ DOI 107717peerj1582 1823

indoors (for example brought in on cut plants) most taxa sampled from houses wereeither scavengers predators or parasitoids Carpet beetles (Dermestidae) were foundfeeding on dog kibble dead insects and nail clippings Other scavengers like silverfish(found in 68 of homes) and book lice were also common Carrion-feeding flesh flies(Sarcophagidae) were found during the study emerging from a rodent killed by a housecat Spiders (including spitting spiders Scytodidae that spit venom up to a centimeterto ensnare prey Foelix 2011) and centipedes (especially Scutigeridae) were the primarypredators sampled Minute parasitoid wasps (especially Eulophidae and Platygastridae sl)that potentially parasitize other household arthropods were also common inhabitants Forinstance one species of Eulophidae Aprostocetus (Tetrastichodes) hagenowii (Ratzeburg)(Table S1) a known parasitoid of blattid cockroach egg cases (oothecae) was commonlycollected in homes as were its hosts Considering the range and abundance of life historiesfound in our study the trophic dynamics of the indoor ecosystem is an area in need offuture study

The rich arthropod diversity we identified from houses reflects a gradient of associationwith human habitations from synanthropic arthropods that appear strongly adaptedto human houses (cobweb spiders carpet beetles book lice) to others that seek shelterand resources only on occasion (ants ground beetles hunting spiders smoky browncockroaches) tomany groups that simply become trapped in houses to their own detriment(leafhoppers gall midges click beetles) Most of the arthropod groups we identified donot have life histories that are known to be closely associated with the indoors Manyarthropods may find themselves indoors as a result of the lsquoMalaise trap effectrsquo houses likeMalaise and other flight intercept traps are effective at capturing local arthropods that maybe travelling through the environment or are attracted to houses by artificial light foodand shelter These arthropods may be active in a house for a short period of time whereinteractions between them and the housersquos residents may occur but eventually they musteither find an exit or succumb to mortality The idea that homes are traps or filters of localoutdoor arthropod fauna implies the importance of further investigating the dynamicsbetween the greater landscape and the indoor environment

Biodiversity in urban landscapes is richer than was once thought (McKinney 2008Fattorini 2011 Fattorini 2014) and we find here that the indoor manufacturedenvironment also supports more diversity than anticipated These findings represent a newunderstanding of the makeup of the indoor arthropod community and their distributionwithin houses Arthropods within our homes are both diverse and prevalent and are amix of closely synanthropic species and a great diversity of species that wander indoorsby accident Many species we found were unexpected unnoticed by residents until theywere collected and play no pestiferous role in human houses Yet further research on theecological dynamics of the indoor biome is needed to understand the potential economicand health implications of the species that live and have evolved in such close proximityto us

Bertone et al (2016) PeerJ DOI 107717peerj1582 1923

ACKNOWLEDGEMENTSWeare verymuch indebted to themany volunteers who allowed us to sample the arthropodsin their homes Kelly Oten aided in designing many aspects of the study and participatedin sampling homes We also thank others who helped collect specimens Nancy Brill MaryJane Epps Clint Penick Amy Savage Patricia Turner and Steven Turner Melissa Howellaided in sorting arthropods

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by National Science Foundation funding DEB 1257960 and NSFCareer 0953350 The funders had no role in study design data collection and analysisdecision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsNational Science Foundation DEB 1257960NSF Career 0953350

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Matthew A Bertone conceived and designed the experiments performed theexperiments analyzed the data wrote the paper prepared figures andor tables revieweddrafts of the paperbull Misha Leong analyzed the data wrote the paper prepared figures andor tables revieweddrafts of the paperbull Keith M Bayless reviewed drafts of the paper specimen Identificationbull Tara LF Malow analyzed the data data Entry amp Managementbull Robert R Dunn conceived and designed the experiments contributed reagentsmateri-alsanalysis tools reviewed drafts of the paperbull Michelle D Trautwein conceived and designed the experiments analyzed the datacontributed reagentsmaterialsanalysis tools wrote the paper reviewed drafts of thepaper

Data AvailabilityThe following information was supplied regarding data availability

Data has been uploaded to the Supplemental Information

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj1582supplemental-information

Bertone et al (2016) PeerJ DOI 107717peerj1582 2023

REFERENCESArauacutejo A Jansen AM Reinhard K Ferreira LF 2009 Paleoparasitology of Chagas

disease a reviewMemoacuterias do Instituto Oswaldo Cruz 1049ndash16DOI 101590S0074-02762009000900004

Arlian LG Bernstein D Bernstein IL Friedman S Grant A Lieberman P LopezMMetzger J Platts-Mills T Schatz M Spector S Wasserman SI Zeiger RS 1992Prevalence of dust mites in the homes of people with asthma living in eight differentgeographic areas of the United States Journal of Allergy and Clinical Immunology90292ndash300 DOI 101016S0091-6749(05)80006-5

Balviacuten O Munclinger P Kratochviacutel L Viliacutemovaacute J 2012Mitochondrial DNA andmorphology show independent evolutionary histories of bedbug Cimex lectularius(Heteroptera Cimicidae) on bats and humans Parasitology Research 111457ndash469DOI 101007s00436-012-2862-5

Baz A Monserrat VJ 1999 Distribution of domestic Psocoptera in Madrid apartmentsMedical and Veterinary Entomology 13259ndash264DOI 101046j1365-2915199900176x

Belles X 1997 Los insectos y el hombre prehistoacuterico BoletAtilden de la Sociedad Entomoloacuteg-ica Aragonesa 20319ndash325

BoothW Santangelo RG Vargo EL Mukha DV Schal C 2010 Population geneticstructure in German cockroaches (Blattella germanica) differentiated islands in anagricultural landscape Journal of Heredity 102175ndash183

Chopard L 1928 Sur une gravure drsquoinsecte de lrsquoepoque magdaleacutenienne Comptes Rendusde la Societeacute de Biogeographie 564ndash67

Colloff MJ 1998 Distribution and abundance of dust mites within homes Allergy5324ndash27 DOI 101111j1398-99951998tb04992x

Colwell RK 2013 EstimateS statistical estimation of species richness and shares speciesfrom samples Version 9 Userrsquos Guide and application Available at http purloclcorg estimates

Committee on Urban Pest Management Environmental Studies Board Commissionon Natural Resources and National Research Council 1980Urban pest manage-ment Washington DC National Academy Press

CranshawW 2011 A review of nuisance invader household pests of the United StatesAmerican Entomologist 57165ndash169 DOI 101093ae573165

Crissman JR BoothW Santangelo RG Mukha DV Vargo EL Schal C 2010Population genetic structure of the German cockroach (Blattodea Blattellidae)in apartment buildings Journal of Medical Entomology 47(4)553ndash564DOI 101093jmedent474553

Diaz-Montano J Campbell JF Phillips TW Throne JE 2014 Evaluation of potentialattractants for Liposcelis bostrychophila (Psocoptera Liposcelididae) Journal ofEconomic Entomology 107867ndash874 DOI 101603EC13427

Bertone et al (2016) PeerJ DOI 107717peerj1582 2123

Dunn RR Fierer N Henley JB Leff JW Menninger HL 2013Home life factorsstructuring the bacterial diversity found within and between homes PLoS ONE8e64133 DOI 101371journalpone0064133

EppsMJ Menninger HL LaSala N Dunn RR 2014 Too big to be noticed crypticinvasion of Asian camel crickets in North American houses PeerJ 2e523DOI 107717peerj523

Fattorini S 2011 Insect extinction by urbanization a long term study in Rome Biologi-cal Conservation 144370ndash375 DOI 101016jbiocon201009014

Fattorini S 2014 Urban biodiversity hotspots are not related to the structure of greenspaces a case study of tenebrionid beetles from Rome Italy Urban Ecosystems171033ndash1045 DOI 101007s11252-014-0375-y

Foelix R 2011 Biology of spiders 3rd edition New York Oxford University Press 432 pGrimaldi D Engel M 2005 Evolution of the insects New York Oxford University Press

755 pGrimaldi D Ginsberg PS Thayer L McEvey S Hauser M Turelli M Brown B 2015

Strange little flies in the big city exotic flower-breeding Drosophilidae (Diptera) inUrban Los Angeles PLoS ONE 10(4)e0122575 DOI 101371journalpone0122575

Hahn JD AscernoME 1991 Public attitudes toward urban arthropods in MinnesotaAmerican Entomologist 37179ndash185 DOI 101093ae373179

Hartop EA Brown BV Disney RH 2015 Opportunity in our ignorance Urbanbiodiversity study reveals 30 new species and one new nearctic record forMegaselia(Diptera Phoridae) in Los Angeles (California USA) Zootaxa 3941451ndash484DOI 1011646zootaxa394141

Heppner JB 2008 Butterflies and moths (Lepidoptera) In Capinera JL ed Encyclope-dia of entomology Amsterdam Springer 626ndash672

How YF Lee CY 2010 Survey of bed bugs in infested premises in Malaysia and Singa-pore Journal of Vector Ecology 35(1)89ndash94 DOI 101111j1948-7134201000063x

Johnson JB Hagen KS 1981 A neuropterous larva uses an allomone to attack termitesNature 289506ndash507 DOI 101038289506a0

Keller A 2007 Drosophila melanogaster rsquos history as a human commensal Current Biology17(3)R77ndashR81 DOI 101016jcub200612031

Kenward H Carrott J 2006 Insect species associations characterise past occupation sitesJournal of Archaeological Science 331452ndash1473 DOI 101016jjas200506018

Kislev ME Hartmann A Galili E 2004 Archaeobotanical and archaeoentomologicalevidence from a well at Atlit-Yam indicates colder more humid climate on theIsraeli coast during the PPNC period Journal of Archaeological Science 311301ndash1310DOI 101016jjas200402010

Klimov PB OrsquoConnor B 2013 Is permanent parasitism reversiblemdashCritical evidencefrom early evolution of house dust mites Systematic Biology 62(3)411ndash423DOI 101093sysbiosyt008

Krantz GWWalter DE 2009 A manual of acarology 3rd edition Lubbock Texas TechUniversity Press

Bertone et al (2016) PeerJ DOI 107717peerj1582 2223

Legner EF McCoy CW 1966 The houseflyMusca domestica Linnaeus as an exoticspecies in the Western Hemisphere incites biological control studies The CanadianEntomologist 98(03)243ndash248 DOI 104039Ent98243-3

McIntyre NE 2000 Ecology of urban arthropods a review and a call to action Annals ofthe Entomological Society of America 93825ndash835DOI 1016030013-8746(2000)093[0825EOUAAR]20CO2

McKinneyML 2008 Effects of urbanization on species richness a review of plants andanimals Urban Ecosystems 11161ndash176 DOI 101007s11252-007-0045-4

NESCentWorking Group on the Evolutionary Biology of the Built EnvironmentMartin LJ Adams RI Bateman A Bik HM Hawks J Hird SM Hughes D KembelSW Kinney K Kolokotronis S-O Levy G McClain C Meadow JF Medina RFMhuireach G Moreau CS Munshi-South J Nichols LM Palmer C Popova L SchalC Taumlubel M TrautweinM Ugalde JA Dunn RR 2015 Evolution of the indoorbiome Trends in Ecology amp Evolution 30223ndash232 DOI 101016jtree201502001

Nielsen BO Mahler V Rasmussen P 2000 An arthropod assemblage and the ecologicalconditions in a byre at the Neolithic settlement of Weier Switzerland Journal ofArchaeological Science 27209ndash218 DOI 101006jasc19990448

Oliver I Beattie AJ 2002 Invertebrate morphospecies as surrogates for species a casestudy Conservation Biology 1099ndash109

Panagiotakopulu E 2001 New records for ancient pests archaeoentomology in EgyptJournal of Archaeological Science 281235ndash1246 DOI 101006jasc20010697

Panagiotakopulu E 2003 Insect remains from the collections in the Egyptian Museumof Turin Archaeometry 45355ndash362 DOI 1011111475-475400113

Panagiotakopulu E 2004 Dipterous remains and archaeological interpretation Journalof Archaeological Science 311675ndash1684 DOI 101016jjas200404008

R Core Team 2015 R A language and environment for statistical computing Vienna RFoundation for Statistical Computing Available at httpwwwR-projectorg

RobinsonWH 2005Urban insects and arachnids a handbook of urban entomology Cambridge Cambridge University Press

Roth LM 1985 A taxonomic revision of the genus Blattella Caudell (DictyopteraBlattaria Blattellidae) Entomologica Scandinavica 221ndash221

Runstrom ES Bennett GW 1990 Distribution and movement patterns of Germancockroaches (Dictyoptera Blattellidae) within apartment buildings Journal ofMedical Entomology 27(4)515ndash518 DOI 101093jmedent274515

Turner BD Bishop J 1998 An analysis of the incidence of psocids in domestic kitchensthe PPFA 1997 household survey (Whatrsquos bugging your kitchen) EnvironmentalHealth Journal 106310ndash314

Whitman DW 2008 The significance of body size in the Orthoptera a review Journal ofOrthoptera Research 17117ndash134 DOI 1016651082-6467-172117

Bertone et al (2016) PeerJ DOI 107717peerj1582 2323