Submitted 18 May 2016Accepted 5 October 2016Published 9 November 2016

Corresponding authorMarius Somveillemariussomveillezoooxacuk

Academic editorScott Edwards

Additional Information andDeclarations can be found onpage 15

DOI 107717peerj2658

Copyright2016 Somveille et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

A global analysis of bird plumagepatterns reveals no association betweenhabitat and camouflageMarius Somveille12 Kate LA Marshall1 and Thanh-Lan Gluckman134

1Department of Zoology University of Cambridge Cambridge United Kingdom2The Edward Grey Institute Department of Zoology University of Oxford Oxford United Kingdom3Department of Animal and Plant Sciences University of Sheffield Sheffield United Kingdom4Center for Interdisciplinary Research in Biology College de France Paris France

ABSTRACTEvidence suggests that animal patterns (motifs) function in camouflage Irregularmottled patterns can facilitate concealment when stationary in cluttered habitatswhereas regular patterns typically prevent capture during movement in open habitatsBird plumage patterns have predominantly converged on just four typesmdashmottled(irregular) scales bars and spots (regular)mdashand habitat could be driving convergentevolution in avian patterning Based on sensory ecology we therefore predict thatirregular patterns would be associated with visually noisy closed habitats and thatregular patterns would be associatedwith open habitats Regular patterns have also beenshown to function in communication for sexually competing males to stand-out andattract females so we predict that male breeding plumage patterns evolved in both openand closed habitats Here taking phylogenetic relatedness into account we investigateecological selection for bird plumage patterns across the class Aves We surveyedplumage patterns in 80of all avian species worldwideOf these 2756 bird species haveregular and irregular plumage patterns as well as habitat information In this subsetwe tested whether adult breedingnon-breeding plumages in each sex and juvenileplumages were associated with the habitat types found within the speciesrsquo geographicaldistributions We found no evidence for an association between habitat and plumagepatterns across the worldrsquos birds and little phylogenetic signal We also found thatspecies with regular and irregular plumage patterns were distributed randomly acrossthe worldrsquos eco-regions without being affected by habitat type These results indicatethat at the global spatial and taxonomic scale habitat does not predict convergentevolution in bird plumage patterns contrary to the camouflage hypothesis

Subjects Biodiversity Ecology Evolutionary Studies ZoologyKeywords Ecological selection Camouflage Plumage patterns Signalling MacroevolutionNatural selection

INTRODUCTIONSelection for optimal camouflage and sexual signals in the different habitats of animalscan drive phenotypic variation (eg Endler 1978 Stuart-Fox amp Ord 2004 Hoekstra et al2006 Rosenblum 2006 Seehausen et al 2008 reviewed in Stevens 2013) Animals exhibit adiversity of pigmentation patterns or motifs (ie stipples) that are predominantly thought

How to cite this article Somveille et al (2016) A global analysis of bird plumage patterns reveals no association between habitat andcamouflage PeerJ 4e2658 DOI 107717peerj2658

to function in camouflage such as by generally matching the background or by breakingup (disrupting) the prey outline and creating false edges to prevent detection by predators(Thayer 1909 Cott 1940 Pough 1976 Stevens amp Merilaita 2009) Under sensory ecologytheory the likelihood of a predator being able to detect its prey depends on how effectivelythe visual cue is transmitted to the predatorrsquos eye and on how well the predatorrsquos specificvisual system can detectrecognise its prey against the background on which it is viewed(eg Endler 1992) Past studies have shown that genetic adaptation of camouflage appearsto enhance backgroundmatching in local environments and increase survival against visualpredators (eg Hoekstra Krenz amp Nashman 2005 Vignieri Larson amp Hoekstra 2010)Crucially visual modelling studies have shown that such local adaptation can preventdetection by the actual visual systems of predators such as hunting birds (eg Stuart-Foxet al 2004Marshall et al 2015aMarshall Philpot amp Stevens 2015b) thus indicating thatcamouflage tends to be optimised to local habitats under natural selection

Across animals different types of visual patterns made up of different patches ofpigmentation to make up an overall pattern or lsquomotifrsquo have been linked to differentfunctions in camouflage Specifically irregular patterns (mottled) tend to function instationary camouflage while those that regularly repeat a pattern or motif (bars spots)function in motion camouflage which are in turn predicted to be more effective in closedand open habitats respectively (Marshall amp Gluckman 2015) Birds are the most welldescribed taxonomic group of animal and can be found in all types of habitats on all majorlandmasses (Gluckman amp Cardoso 2010 Jetz et al 2012) making them particularly wellsuited for investigating sensory ecology hypotheses Recent studies on bird colourationacross a large number of species and at large spatial scale revealed that islands are associatedwith reduced signal intensity (Doutrelant et al 2016) and that colour heterogeneitydecreases with body size (Galvan et al 2013) but also showed distinct effects of habitatlife history and sexual selection on the evolution of colouration that lacks patterning(an absence of patterns or uniform colouration) such as bright red carotenoid and dullbrown melanins (Dale et al 2015 Dunn Armenta amp Whittingham 2015) However nostudy has yet explicitly examined the role of habitat and camouflage on avian featherpatterns type at the global scale (but see Riegner 2008 Gluckman amp Cardoso 2010)

In spite of the spectacular diversity in phenotypes across the class Aves bird plumagepatterns have predominantly converged on just four types mottled scales bars and spots(Fig 1 Gluckman 2014 Marshall amp Gluckman 2015 Gluckman amp Mundy 2016) Moststudies of camouflage focus on single or few species (Marshall amp Gluckman 2015) thatmay not be representative of broad scale selection pressures Here we investigated whethersensory ecology theory could explain convergent evolution in the camouflage plumagepatterns of birds at the global spatial and taxonomic scale ie with a global spatial extentusing large spatial units and data on most land bird species

It is thought that irregular patterns function in the camouflage of stationary animalsthrough background matching and disruptive camouflage in order to evade detectionby predators (Thayer 1909 Cott 1940 Endler 1978 Bradbury amp Vehrencamp 1998)Accordingly static irregular camouflage patterns are harder to detect when viewed againstmore cluttered backgrounds containing distractors (eg Dimitrova amp Merilaita 2009)

Somveille et al (2016) PeerJ DOI 107717peerj2658 222

Figure 1 The predominant types of plumage patterns in birds (A) Irregular mottled plumage con-sists of feathers that are heterogeneously pigmented (Jungle NightjarndashCaprimulgus indicus indicus) Reg-ular plumage patterns can be comprised of (B) scales where pigmentation follows the edge of the vane(MallardndashAnas platyrhynchos) (C) bars that are made of alternating dark and light pigmentation transver-sal to the feathers axis (Andean flickerndashColaptes rupicola) and (D) spots where one or more spots pigmenteach feather (GuineafowlndashNumida meleagris) Photos Grey Nightjarjpg by Koshy Koshy (retrieved fromhttpscommonswikimediaorgwikiFileGrey_Nightjarjpg CC BY 20 license) Female Mallard DuckRestjpg by Alain Carpentier (retrieved from httpscommonswikimediaorgwikiFileFemale_Mallard_Duck_Restjpg under a CC-BY-SA 30 license) Colaptes rupicola 20070123jpg by Adam Kumiszcza (re-trieved from httpsenwikipediaorgwikiAndean_flickermediaFileColaptes_rupicola_20070123jpg under a CC-BY-SA 30 license) and Pintade de Numidiejpg by JP Hamon (retrieved from httpscommonswikimediaorgwikiFilePintade_de_Numidiejpg under a CC BY-SA 30 license) respectively

Therefore irregular patterns should be favoured in visually complex closed environmentsthat provide backgrounds where a prey animal can easily blend in Irregular mottledpatterns are common in avian species and are more frequently found in females andjuveniles in comparison to regular barred plumage patterns (Gluckman amp Cardoso 2010)

Current evidence suggests that regular patterns such as bars and spots typicallyfacilitate camouflage during movement and therefore function as a secondary defenceduring the escape of prey by exploiting specific features of receiver visual acuity This typeof camouflage would include motion dazzle whereby highly contrasting patterns preventpredators from estimating the speed and direction of moving prey (eg Scott-Samuelet al 2011 Stevens Yule amp Ruxton 2008 Stevens et al 2011 Von Helversen Schooler ampCzienskowski 2013 How amp Zanker 2014 Hughes Troscianko amp Stevens 2014) as well asflicker-fusion camouflage in which the patterns of a moving animal become blurred

Somveille et al (2016) PeerJ DOI 107717peerj2658 322

to the predatorrsquos vision so that it appears to match the background against which it ismoving (eg Brodie 1989 Brodie 1992 Brodie 1993 Lindell amp Forsman 1996) Giventhat escape by flight requires space and that motion camouflage is dependent on effectivetransmission to the predatorrsquos eye regular patterns in birds should be more commonin open habitats where patterns are easily visible and escape by flight is unencumberedAdditionally regular patterns may have a dual function in both camouflage and visualcommunication with conspecifics (Marshall 2000 Gluckman amp Cardoso 2010) and dueto multiple functions may evolve independently of habitat in adult males (Bradbury ampVehrencamp 1998 Endler 1992 Kenward et al 2004 Leal amp Fleishman 2004 Seehausen etal 2008McLean Moussalli amp Stuart-Fox 2014)

Across the world habitats differ in their structural composition eg forested habitats arecluttered and visually noisy while desert habitats are not The dorsal plumage patterns ofbirds are likely to function in camouflage in adults of both sexes as well as juveniles whereasa communication function is likely to evolve on the ventral surface of sexually competingmales (Stuart-Fox amp Ord 2004 Gluckman amp Cardoso 2010 Garcia Rohr amp Dyer 2013)

In this study we investigated whether habitat selects for convergent evolution in theplumage patterns of terrestrial birds at the global scale using the geographical distributionof all known avian species (excluding sea birds) Firstly we looked for an associationbetween plumage patterns type and habitat type across avian species and secondly weinvestigated whether patterned species were distributed at random across the world Weexpected to find a significant association between closed and open habitats with irregularand regular patterns respectively in the plumage of adults as well as juveniles In thesexually selected ventral plumage of breeding males we expected that plumage patternevolution would be independent of habitat due to its function in communication Inaddition we expected the distribution of irregularly and regularly patterned species acrossgeographical space to differ from random and be affected by habitat

MATERIAL AND METHODSData collectionWe focused on the most prominent aspect of patterning the four different types of spatialarrangement of pigmentation (Fig 1) To collect plumage pattern information we referredto field guides covering all major landmasses North and Central America (Sibley 2000VanPerlo 2006) South America and Antarctica (De La Pena amp Rumboll 1998 Restall Rodneramp Lentino 2007) sub-Saharan Africa and Madagascar (Langrand 1990 Sinclair amp Ryan2003) Europe North Africa and Central Asia (Heinzel Fitter amp Parslow 1995 GrimmettInskipp amp Inskipp 1999 Arlott 2007 Arlott 2009 Brazil 2009) East and South-East Asia(MacKinnon amp Phillips 1993 Coates amp Bishop 1997 Robson 2005) and Oceania (BeehlerPratt amp Zimmerman 1986 Pratt Bruner amp Berrett 1987 Simpson amp Day 2004 Robertsonamp Heather 2005) Where multiple subspecies were present we collected information onthe nominate subspecies Overall we examined 8006 avian species (80 of class Aves) tocategorize their patterning Juvenile plumages are less frequently drawn in field guides sowe were only able to categorise juvenile plumage information in 2603 species (26 of class

Somveille et al (2016) PeerJ DOI 107717peerj2658 422

Aves) Species that were unpatterned andor without habitat information were excludedfrom further statistical analyses giving an overall sample size of 2756 avian species (34of the species considered) providing information for 2593 adult and 2104 juvenile avianspecies (see the list of species in Appendix S1)

We scored the plumage of both sexes as well as juveniles of each species for an absenceof patterns mottled scaled barred and spotted patterns both on the ventral and dorsalsurface separately (Fig 1) Irregular mottled patterns were defined as pigmentation thatdid not have a clearly discernible motif or the putative motif had irregular borders asfrequently found on the dorsum of sparrows (in contrast with the stripes of species fromthe genus Gavia that have clear and neat boundaries in the stripes on the neck) Regularpatterns had a motif with regular borders and were repeated across a patch of patterning(Fig 1) Some species havemultiple patterns on either the ventral or dorsal surface (eg themale zebra finch Taeniopygia guttata has barred patterns on the breast and spotted flanks)on the ventral surface 62 and 64 species for males during the non-breeding and breedingseasons respectively 70 and 72 species for females during the non-breeding and breedingseasons respectively and 63 species for juveniles and on the dorsal surface 229 and 222species for males during the non-breeding and breeding seasons respectively 231 and 233species for females during the non-breeding and breeding seasons respectively and 102species for juveniles In these types of species all of the different types of plumage patternson each surface were scored and each pattern type was analysed separately Where speciesexhibited variable patterns between moults we collected the breeding and non-breedingplumage given that there may be variation in selection pressure on the different types ofpatterns exhibited Squares triangles and stripes also occur within the plumage of birds butare comparatively rare (eg out of these three rare patterns stripes are the most common43 species) Stripes are comprised of regular longitudinal lines (unlike bars which arepigmented transversal to the feathers axis) These rare types of patterns were excluded fromthe analysis due to low statistical power

We examined all of the combinations of genderage (malefemalejuvenile) season(breedingnon-breeding) and body part (ventraldorsal) individually Herein we refer toeach as biological combinations

Species geographical distributionsGlobal geographical distributions of all avian species were obtained from BirdlifeInternational amp NatureServe (2012) for all species in the plumage dataset and treatedas described in Somveille et al (2013) Briefly the polygons in the dataset represent theglobal distribution of species and we included only the polygons for which species presencewas coded as extant or probably extant and the species origin was coded as native orreintroduced and we excluded the polygons corresponding to species in passage (ieduring migration) In addition breeding distributions (defined as polygons correspondingto the areas where they are present only during the breeding season) were analysedseparately from non-breeding distributions (defined as polygons where they are presentonly during the non-breeding season) We focused solely on land birds as the geographical

Somveille et al (2016) PeerJ DOI 107717peerj2658 522

distribution ofmarine species is not well known and represents less than 3of avian speciesWe statistically examined our data for an association between habitat and plumage

patterns for each biological combination For adult breeding and non-breeding plumages weused the breeding and non-breeding geographical distributions of bird species respectivelyFor juvenile plumages we used the breeding geographical distributions as this life stageoccurs predominantly during the adult breeding season Note that for resident species(ie non-migrants 85 of avian species) the breeding and non-breeding geographicaldistributions are the same Irregular patterning is found in 24 of the 8006 avian speciesanalysed (1887 species) whereas regular patterning is found in 23 (1858 species) Of theregular patterns (scaled barred and spotted) scaled and spotted patterns are prevalent in25 (470 species) and 30 (549 species) of avian species (across biological combinations)respectively whereas barring is observed in 66 (1220 species) of avian species (acrossbiological combinations)ndashpercentages are relative to the number of species with regularplumage patterns in at least one biological combination

To avoid an underestimation or overestimation of ecological signal for regular patternswe categorized regular patterns in twoways for our analyses (1) all regular patterns groupedtogether as a single category and (2) just barred plumage patterns due to these being themost frequent type of regular pattern occurring in bird plumage patterns (Gluckman ampCardoso 2009 Gluckman amp Cardoso 2010) The results were qualitatively the same for theanalyses of regular patterns together and barred plumage patterns alone and we presentthe results for the category of all regular patterns together (a comparison of mottled versusbarred patterns for all analyses are available in the Supplemental Information 1)

Phylogenetic comparative analysisTo examine the habitat in which species live we analysed the habitat types found withintheir geographical distributions For each species with irregular or regular plumage patternswe quantified how open or closed is the habitat in which they live a measure herein calledhabitat coverage Information on habitat was obtained from the global MODIS land coverdataset (Channan Collins amp Emanuel 2014) We coded forests pixels as closed habitat witha value of 1 savannas grasslands wetlands croplands snow and ice and barren or sparselyvegetated pixels as open habitat with a value of 0 and shrublands woody savannas andcroplandnatural vegetation mosaic pixels as partially closed habitat with a value of 05For each species we then quantified habitat coverage as the average habitat value acrossthe pixels found within the speciesrsquo geographical distribution This allowed us to obtain acontinuous measure of habitat for each species during both its breeding and non-breedingseasonsndashwhich can be very different for migrants representing sim16 of avian species(Somveille et al 2013) We then removed species for which no habitat information wereavailable and no plumage patterns were present

Plumage patterns may be phylogenetically conserved resulting in similar plumagepatterns occurring in closely related species due to phylogenetic inertia (Felsenstein 1985Revell Harmon amp Collar 2008) rather than caused by habitats selection In addition thetendency of species to resemble related species more so than randomly selected speciesfrom a tree breaks the assumption of independence of ordinary least square models (Revell

Somveille et al (2016) PeerJ DOI 107717peerj2658 622

2010) We therefore examined the association between plumage patterns and habitat byperforming comparative analyses that take phylogenetic relatedness into account

For each biological combination we computed a phylogenetic logistic regression model(Ives amp Garland Jr 2010) with plumage pattern type (regular vs irregular regular pattern= 0 and irregular pattern = 1) as the dependent variable and habitat coverage as theexplanatory variable (R code phyloglm(plumage pattern type sim habitat coverage phy= tree method = lsquolsquologistic_IG10rsquorsquo)) For each biological combination the analysis wasperformed only using species with plumage patterns (regular or irregular) As nophylogenetic signal was detected in the models we also employed standard generalizedlinear models (GLMs) for comparison (R code glm(plumage pattern type sim habitatcoverage family= lsquolsquobinomialrsquorsquo)) At large sample sizes trivially small effects can be detectedTherefore to examine the statistical significance of the relationship for the GLMs weevaluated this significance by assessing the goodness-of-fit using the McFaddenrsquos pseudo-R2 (McFadden 1974) All statistical analyses were performed in R (R Development CoreTeam 2012) phylogenetic logistic regressions were performed using the phylolmR package

Phylogenetic information for bird species was obtained from httpBirdTreeorg (Jetz etal 2012) This phylogeny randomly resolves species with missing data by assuming mono-phyletic genera To account for phylogenetic uncertainties we performed our statisticalanalyses (ie phylogenetic logistic regression models) on 100 randomly selected trees andreported the observed variation in the parameter estimates Branch lengths were computedusing the Grafen method (Grafen 1989 R function computebrlen) In phylogeneticlogistic regressions a captures the phylogenetic signal in the data and can vary betweenminus4 (no phylogenetic signal) and 4 (strong phylogenetic signal Ives amp Garland Jr 2010)

Eco-region avian assemblage analysisTo investigate whether species with regular and irregular plumage patterns were distributedrandomly across the world we examined avian assemblages at the scale of the eco-region(Olson et al 2001) using a global map of the worldrsquos terrestrial eco-regions made availableby The Nature Conservancy (2009) (Fig S1B) The physical component that defines habitattype are the individual units of land (eco-regions) containing habitat type specific plantcommunities and species nested within biomes (Olson et al 2001) We categorizedhabitat into two main types closed and open Closed habitat was defined as broadleafand coniferous forests as well as Mediterranean forests and the Taiga and open habitatcomprised the various types of grasslands deserts and tundra as well as the scarce habitatsof Inland water Rock and ice Mangrove habitat was not considered in our analysis as itis not clearly composed of solely closed or open habitat

A bird species was classed as occurring in a given eco-region if its mapped rangeoverlapped with any part of the eco-region Although this is a coarse species geographicaldistribution it represents a good approximation of occurrence given the spatial resolutionof the eco-regions (Hurlbert amp Jetz 2007) Species richness was measured as the numberof species occurring in a given eco-region After removing eco-regions in which no birdspecies occur 791 eco-regions remained of which 293 (37) were composed of openhabitat and 498 (63) of closed habitat

Somveille et al (2016) PeerJ DOI 107717peerj2658 722

To examine whether the composition of plumage patterns in avian assemblages acrossthe worldrsquos eco-regions was random or affected by habitat type we quantified the ratio ofregular to irregular patterns in each eco-region and compared it to a null expectation basedon random distribution of the species The ratio was calculated as the number of specieswith regular patterns divided by the number of species with irregular patterns (hereinreferred to as ratio regular-irregular) For the analysis comparing barred and mottledpatterns the ratio was calculated as the number of barred species divided by the number ofmottled species (results are presented in Supplemental Information 1) To avoid a skew inthe distribution we log transformed this ratio for all of the analyses Eco-regions withoutany species with an irregular plumage pattern (26 of the eco-regions on average acrossthe biological combinations) were excluded from this analysis because the ratio could notbe calculated

The null distribution of plumage pattern ratios across the worldrsquos eco-regions wasgenerated by drawing species without replacement 100 times from the hemisphericalspecies pool (ie treating Western and Eastern Hemispheres separately) In each eco-region we drew a number of species corresponding to the observed species richness of thelocal assemblage and identified eco-regions with significantly high or low values to thenull expectation

To take spatial autocorrelation into account ndashwhereby species occurring in the localpool of species (ie in the neighbouring eco-regions) are more likely to occur in the focaleco-region ndashwe weighted the probability of sampling species based on their degree ofoccurrence in the local pool In each avian assemblage (ie eco-region) for each speciesin the hemispherical pool we determined the proportion of neighbouring eco-regions inwhich it occurs Then for each discrete proportion (ie because each eco-region has adiscrete number of direct neighbours) we calculated the proportion of species occurringin the focal eco-region For example for a given focal eco-region among all of the speciesoccurring in 50 of the adjoining neighbours 30 of these species also occur in the focaleco-region We then fitted a non-linear model (using the nls function in R) to estimate theparameters of this relationship across all the eco-regions (treating the western and easternhemispheres separately) The fitted curve was then used to determine the probability of aspecies to occur in a focal eco-region given its occurrence in the neighbouring eco-regions(ie the local pool)

We examined the species of theWestern hemisphere (the Americas defined as longitudeltminus30W) separately from the Eastern hemisphere (the Old World defined as longitudegtminus30W) as they have distinctive avian species pools For example the total ratioregularndashirregular (as well as the total ratio barredndashmottled) is different between thesetwo hemispheres (see Table S2 and Fig S3) The global species pool from which specieswere drawn was therefore separated into two species pools representing each hemisphere

Following the camouflage hypothesis we expect the ratio regularndashirregular to be higherin open habitats than the expected null values (eg regular patterns dominate) and tobe smaller than the null expectation in closed habitats (eg irregular patterns dominate)To test this hypothesis we computed a p-value by comparing the observed value to thedistribution of null values If the eco-region was composed of open habitat we used

Somveille et al (2016) PeerJ DOI 107717peerj2658 822

1 minus the cumulative probability because we expect the ratio regular-irregular tobe higher than the null expectation To account for multiple testing (ie one test foreach eco-region) we controlled the false discovery rate using the method developed byBenjamini amp Hochberg (1995)

RESULTSAll types of plumage patterns are found in all biological combinations of females malesand juveniles for non-breeding and breeding plumage on both the ventral and dorsalsurface (Table S1) Mottled plumage is the most prevalent plumage pattern and is foundon the dorsal surface more frequently than on the ventral surface in all sexage classesand is least frequent in males Barred patterns are also common and are frequently foundon the ventral surface of breeding adult males but also in juveniles Scaled and spottedpatterns are less prevalent and are frequently biased towards the dorsal surface of adultsand the ventral surface of juveniles However spotted patterns are also frequently foundon the ventral surface of breeding males and females

Phylogenetic comparative analysisFigure 2 shows very little difference in habitat coverage between species with regular versusirregular plumage patterns for all biological combinations which was confirmed by thestatistical models (Table 1) Phylogenetic uncertainty due to randomly resolving specieswith missing data by assuming monophyletic genera did not meaningfully affect the results(Table 1) For all biological combinations of plumage patterns a was very nearly minus4indicating that almost no phylogenetic signal could be detected in the data for plumagepatterns Due to the lack of phylogenetic signal estimates of intercepts and slopes werealmost identical between phylogenetic logistic regressions and GLMs (Table 1) Althoughmost slopes were significantly different from the null hypothesis for both phylogeneticlogistic regressions and GLMs the association between plumage pattern type and habitatcoverage using GLMs yielded extremely low R2 values (0001ndash0039) with a median R2

of 00065 (Table 1) In addition to the low explanatory power all the models showed anegative relationship between plumage patterns and habitat coverage indicating that regularpatterns are more associated with closed environments relatively to irregular patterns thatare more associated with open environments contrary to the camouflage hypothesis

Eco-region avian assemblage analysisAcross the worldrsquos eco-regions and age sex and breeding combinations avian assemblageshad similar proportions of species with regular and irregular plumage patterns regardlessof habitat type (Fig 3 Fig S2) In addition all eco-regions contained qualitatively thesame ratio of species with and without plumage patterns for each biological combinationregardless of habitat type (Fig 3 Fig S3)

The observed ratio regularndashirregular in the eco-regions of both open and closed habitatsrarely differed from the null expectation (Table 2 similar results were obtained for the ratiobarred-mottled Table S4) Less than 1 of eco-regions with species of birds with patternshad a ratio regularndashirregular significantly lower than the null expectation for any biologicalcombination (Table 2) and most of these eco-regions were located on islands

Somveille et al (2016) PeerJ DOI 107717peerj2658 922

Breeding season Non-breeding season

Ventral Dorsal Ventral Dorsal

Hab

itat c

over

age

Male

Female

Juvenile

00

02

04

06

08

10

Unpatterned Irregular Regular

00

02

04

06

08

10

Unpatterned Irregular Regular

00

02

04

06

08

10

Unpatterned Irregular Regular

00

02

04

06

08

10

Unpatterned Irregular Regular

00

02

04

06

08

10

Unpatterned Irregular Regular

00

02

04

06

08

10

Unpatterned Irregular Regular

00

02

04

06

08

10

Unpatterned Irregular Regular

00

02

04

06

08

10

Unpatterned Irregular Regular00

02

04

06

08

10

Unpatterned Irregular Regular

00

02

04

06

08

10

Unpatterned Irregular Regular

Figure 2 Comparison of habitat coverage values for species without plumage patterns species with ir-regular plumage patterns and species with regular plumage patterns across the class Aves The compar-ison was plotted for all biological combinations

Prop

ortio

n of

spe

cies13

Dorsal13

Ventral13

Male13 Female13 Juvenile13

Patterned13Closed habitat13Open habitat13 Irregular

vs regular13Patterned13 Irregular

vs regular13Patterned13 Irregular

vs regular13

1 2 3 4

00

02

04

06

08

10

1 2 3 4

00

02

04

06

08

10

1 2 3 4

00

02

04

06

08

10

00

02

04

06

08

10

00

02

04

06

08

10

00

02

04

06

08

10

Figure 3 Comparison of the proportion of species with plumage patterns versus without and with ir-regular versus regular patterns in breeding males and females as well as juveniles over the dorsal andventral surface of land birds The Patterned boxplots correspond to the proportion of patterned species ineco-regionsrsquo avian species assemblages The Irregular vs regular boxplots correspond to the proportion ofirregular versus regular patterns in eco-regionsrsquo avian species assemblages for the indicated agesex classThe boxplots in red correspond to closed habitat and the blue boxplots correspond to open habitat

Somveille et al (2016) PeerJ DOI 107717peerj2658 1022

Table 1 Relationship between plumage pattern type (regular versus irregular) and habitat (using our habitat coverage measure) across theclass Aves using Phylogenetic Logistic Regressions (PhyLoRegs) and Generalized Linear Models (GLMs) We present the estimate of the intersectas well as the slope and its associated p-value for both PhyLoRegs and GLMs For PhyLoRegs values correspond to the mean of 100 runs using ran-domly sampled phylogenetic trees from Jetz et al (2012) and values in brackets correspond to the standard deviation Positive slopes indicate thatregular patterns are more associated with open habitat while irregular patterns are more associated with closed habitat and negative slopes indicatethe opposite a is the phylogenetic correlation parameter calculated from the PhyLoRegs R2 values were computed for the GLMs and correspond tothe McFaddenrsquos pseudo-R2

Biological combination PhyLoRegs results GLMs results

Sex Body part Season Rawnumber ofspecies

Intercept Slope P-value a Intercept Slope P-value McFaddenrsquospseudo-r2

Female Ventral NB 1655 0058(lt10minus4)

minus0298(lt10minus4)

0001(lt10minus4)

minus3993(0016)

0058 minus0298 0067 0001

BR 1658 0102(lt10minus4)

minus0375(lt10minus4)

lt0001(lt10minus4)

minus3984(0026)

0101 minus0375 0022 0002

Dorsal NB 1643 0769(lt10minus4)

minus1127(lt10minus4)

lt0001(lt10minus4)

minus3986(0018)

0769 minus1127 lt0001 0021

BR 1648 0786(lt10minus4)

minus1163(lt10minus4)

lt0001(lt10minus4)

minus3983(0026)

0786 minus1163 lt0001 0022

Male Ventral NB 1336 0171(lt10minus4)

minus0532(lt10minus4)

lt0001(lt10minus4)

minus3983(0022)

0171 minus0532 0003 0005

BR 1334 0147(lt10minus4)

minus0575(lt10minus4)

lt0001(lt10minus4)

minus3973(0032)

0147 minus0575 0002 0005

Dorsal NB 1502 0843(lt10minus4)

minus1457(lt10minus4)

lt0001(lt10minus4)

minus3993(0016)

0843 minus1457 lt0001 0036

BR 1478 0901(lt10minus4)

minus1553(lt10minus4)

lt0001(lt10minus4)

minus3989(0023)

0901 minus1553 lt0001 0039

Juvenile Ventral 1443 0384(lt10minus4)

minus0347(lt10minus4)

lt0001(lt10minus4)

minus3981(0029)

0384 minus0347 0047 0002

Dorsal 1394 0700(lt10minus4)

minus0676(lt10minus4)

lt0001(lt10minus4)

minus3985(0016)

07 minus0676 lt0001 0008

NotesSeasonNB Non-breeding BR Breeding

DISCUSSIONAll types of plumage patterns have evolved in juveniles females and males in non-breedingand breeding plumage on both the ventral and dorsal surface (Table S1) and species withregular plumage patterns did not differ on average in the type of habitat in which theyoccur from species with irregular plumage patterns (Table 1 Fig 2) In fact contrary toprevailing sensory ecology based hypotheses of the function of patterns in camouflage wedid not find convincing evidence of an association between habitat type and bird plumagepatterns at the global spatial and taxonomic scale (Table 1 Table S2) In addition we foundthat species with regular and irregular plumage patterns are distributed at random acrossthe worldrsquos eco-regions with respect to one another without any significant effect of theeco-regionsrsquo habitat type

Irregular patterns which tend to function in stationary camouflage are unexpectedlyfound in similar proportion in both closed as well as open habitats that have uniform

Somveille et al (2016) PeerJ DOI 107717peerj2658 1122

Table 2 Assemblage-level test of an association with habitat type for the ratio regular-irregular For each biological combination we present thetotal number of eco-regions that have avian species with plumage patterns and the number proportion and habitat type of eco-regions that have anobserved ratio regular-irregular significantly different from the null expectation

Biological combination Significant eco-regions

Sex Body part Season Number of eco-regions

Number Proportion Name

Female Ventral NB 766 2 0003 Antipodes Subantarctic IslandsTundra (TundrandashAustralasia)Pantanal (FGSndashNeotropics)

BR 759 0 0 ndashDorsal NB 769 0 0 ndash

BR 759 1 0001 New Caledonia Rain Forests(TMBFndashAustralasia)

Male Ventral NB 773 0 0 ndashBR 767 2 0003 Victoria Basin Forest-Savanna

Mosaic (TMBFndashAfrotropics)Kinabalu Montane Alpine Mead-ows (MGSndashIndo-Malay)

Dorsal NB 773 2 0003 Banda Sea Islands MoistDeciduous Forests (TMBFndashAustralasia) New Britain-NewIreland Montane Rain Forests(TMBFndashAustralasia)

BR 767 6 0008 Admiralty Islands Lowland RainForests (TMBFndashAustralasia)Banda Sea Islands MoistDeciduous Forests (TMBFndashAustralasia) New CaledoniaDry Forests (TDBFndashAustralasia)Kinabalu Montane AlpineMeadows (MGSndashIndo-Malay)Fiji Tropical Moist Forests(TMBFndashOceania) Bohai SeaSaline Meadow (FGSndashPalearctic)

Juvenile Ventral 763 1 0001 Antipodes Subantarctic IslandsTundra (TundrandashAustralasia)

Dorsal 761 2 0001 Zambezian Halophytics (FGSndashAfrotropics) Kinabalu MontaneAlpine Meadows (MGSndashIndo-Malay)

NotesHabitat typeTMBF Tropical and Subtropical Moist Broadleaf Forests TDBF Tropical and Subtropical Dry Broadleaf Forests MGS Montane Grasslands and Shrublands MFWSMediterranean Forests Woodlands and Scrub FGS Flooded Grasslands and Savannas DXS Deserts and Xeric ShrublandsSeasonNB Non-breeding BR Breeding

backgrounds (eg deserts) where irregular patterns would probably be easier to detect (egBradbury amp Vehrencamp 1998 Dimitrova amp Merilaita 2009 Hall et al 2013) Contrary toour predictions regular patterns are also found in similar proportion inmore visually noisyclosed habitats where limited space and obstructed transmission would make it difficult toinvoke their function inmotion dazzleflicker-fusion camouflage (eg Brodie 1989 Brodie

Somveille et al (2016) PeerJ DOI 107717peerj2658 1222

1992 Brodie 1993 Lindell amp Forsman 1996 Stevens Yule amp Ruxton 2008 Scott-Samuel etal 2011 Von Helversen Schooler amp Czienskowski 2013 How amp Zanker 2014)

The finding that habitat had no effect on the presence of regular patterns on the ventral(breeding) surface of males (in particular barred patterns Gluckman amp Cardoso 2010)would be expected under sexual selection if regular patterns function solely to maximiseconspicuousness to conspecifics However visual signals should diverge in biologicalhotspots due to species recognitionsexual selection (Bradbury amp Vehrencamp 1998)Habitat may influence whether the pattern stands out against its background for exampleby being conspicuous against a uniform background or opposing the geometric pattern ofthe background Indeed signalling traits can be correlated with ecological characteristics todrive signal divergence such as in African cichlid fish and Anolis lizards (Leal amp Fleishman2004 Seehausen et al 2008) as well as in birds (Doutrelant et al 2016) Other factors suchas whether the pattern is able to convey aspects of individual quality would influence theirevolution independent of the viewing background This perhaps may explain why barredpatterns have repeatedly evolved independently on the ventral surface of males (Gluckmanamp Cardoso 2010) Conceivably the same forces of sexual selectionspecies recognition mayhave shaped the evolution of the other types of patterns in males such as spotted patterns(Roulin et al 2000 b Petrie amp Halliday 2008 Muck amp Goymann 2011 Peacuterez-RodriacuteguezJovani amp Mougeot 2013)

Several factors could explain the seemingly random distribution of regular and irregularplumage patterns from deserts to tropical forests First it could be due to the coarse scaleat which we investigated the association between habitat and plumage patterns Many ofthe empirical studies that demonstrate a camouflage function of patterns in non-colourchanging animals show an association in one or a limited number of species (eg Lovellet al 2013 Kang et al 2014 Marshall Philpot amp Stevens 2015b Wilson-Aggarwal et al2016) or were found via predatorndashprey computer simulations (eg Stevens Yule amp Ruxton2008 Stevens et al 2011 Scott-Samuel et al 2011 Troscianko et al 2013 How amp Zanker2014 Hughes Troscianko amp Stevens 2014 reviewed in Marshall amp Gluckman 2015) At thelevel of microhabitats some studies demonstrate that individual behaviours may facilitatecamouflage such as a behavioural choice to rest on backgrounds that enhance camouflage(Tsurui Honma amp Nishida 2010 Lovell et al 2013 Kang et al 2014 Marshall Philpotamp Stevens 2015b Troscianko et al 2016 Wilson-Aggarwal et al 2016) Under currentcamouflage theorymicrohabitat usage in closed and open habitats should result in irregularpatterning being associated with all habitats as it is typically invoked in static camouflageHowever as regular patterns in camouflage are activated by motion they would verylikely need to be associated with only open habitats Yet no association was found at thescale we investigated and both irregular and regular patterns were randomly distributedand showed no difference in their geographic distribution with uniformly coloured avianspecies and no difference between any biological combination (Figs 2 and 3 Table 1)

In addition the visual sensitivities of potential observers can alter the visual affect ofpatterns in different environments which we did not consider here For example in reeffish regular patterns become blurred at a distance and match the background to preventdetection by fish predators (Marshall 2000) and certain patterns are imperceptible to some

Somveille et al (2016) PeerJ DOI 107717peerj2658 1322

visual systems and may be highly visible to others in certain environments (eg CummingsRosenthal amp Ryan 2003 Siebeck et al 2010) Thus avian camouflage patternsmay be tunedto deceive predatorsrsquo visual systems in certain environments by distance-dependent effectsand by exhibiting signals that predator visual systems cannot detect (private communicationchannels) However to create a distance-dependent effect regular patterns would requirespace to blur the pattern and should therefore have been associatedwithmore open habitatsespecially on the dorsal surface of females and juveniles which was not what we found

Perhaps the use of different strata in the vegetation eg ground-dwelling vs arborealmay present different visual microhabitat backgrounds that alter the selection for patterntype The tops of trees are more open and may allow for more movement required formotion-dazzleflicker-fusion regular patterns whereas ground-dwelling species may benefitfrom background matching irregular patterning Similarly open habitat such as savannahsand grasslands contain patches of closed environment such as bushes and isolated trees inwhich static camouflage via irregular plumage patterning might be favoured Moreovermore closed habitats will be darker due to shade and predator risk might be lower due toreduced visual perception and increased clutter so perhaps camouflage in highly clutteredenvironments is less likely to be favoured by selection Conversely in open environmentsboth regular and irregular patterns are likely to be found for dual functions in camouflageand communication

Developmental constraint may also explain repeated convergence of the four types ofplumage patterns independent of function For example white patches of plumage canbe attributed to morphogen production (Price amp Pavelka 1996) and body size may benegatively related to plumage colour heterogeneity in birds (Galvan et al 2013) Riegner(2008) was the first to study the recurrence of plumage pattern elements across the classAves and emphasised developmental constraint as a mechanism of parallelism rather thanconvergence However patches of pigmentation over the body (eg counter shading)were the major focus of this study and so scales were not included and spots were largelygroupedwith drabblended plumage The results of Riegnerrsquos study demonstrated that someplumage patterns shift along a trajectory correlated with body size and that neither habitatnor common descent adequately predicted the evolution of patches of bold pigmentationover the body in aquatic or marine habitats Also striped (mottled) patterns appeared to bemore frequent in Passerines whereas bars are more prevalent in large bodied species egGalliformes raptors etc However Riegnerrsquos (2008) analysis did not control for phylogenyBased on a theoretical model of reactionndashdiffusion based plumage pattern formation(Prum ampWilliamson 2002) the evolutionary trajectory of plumage in Anseriformes andGalliformes followed the same pathways within and between patches of plumage over thebody (Gluckman amp Mundy 2016) Given that Anseriformes and Galliformes are diverse inlife history attributes this result warrants further investigation at the macroevolutionaryscale Nevertheless these studies indicate that there may be developmental constraint inplumage pattern evolution that may have implications for natural selection

Few patterns may be enough to reduce predation by increasing the number of predatorsearch images which may also favour polymorphisms within species For example thereis frequency-dependent selection on alternative morphs of Tetrix subulata grasshoppers

Somveille et al (2016) PeerJ DOI 107717peerj2658 1422

where each morph has varying amounts of mottled patterns in varying colours Howeverwhen all morphs are present in a population all morphs benefit by providing variation inthe search image of predators (Karpestam Merilaita amp Forsman 2014) In the case of birdsperhaps the four different types of patterns in the context of a community of avian speciesthat may also comprise uniform coloration without patterns may benefit all memberspecies Although intraspecific polymorphism is quite different to interspecific variationintraspecific polymorphism via adaptation to different habitats may be the first step tospeciation leading to interspecific variation (reviewed in Boughman 2002 Stevens 2013McLean amp Fox 2014)

In summary we found no convincing evidence for an association between habitat typeand plumage pattern in land birds worldwide and the distribution of plumage patternsacross the world appears to be random rather than affected by habitat type These resultsopposes the hypothesis that closed habitat should contain more species with irregularplumage pattern and open habitat more species with regular plumage pattern as a resultof habitat selection for camouflage This is an intriguing result that implies that plumagepattern evolution does not conform to the prevailing views of selection for camouflage atthe global spatial and taxonomic scale

ACKNOWLEDGEMENTSWewould like to thank Trevor Price and two anonymous reviewers for insightful commentsas well as John A Endler Nicholas I Mundy Fabien Laroche and Andrea Manica forthoughtful feedback as well as Dieter Lukas for technical advice on comparative approaches

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis research was funded by an Entente Cordiale Scholarship to MS a Biotechnology andBiological Sciences Research Council studentship to KLAM and the Cambridge OverseasTrust to T-LG 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 authorsEntente Cordiale ScholarshipBiotechnology and Biological Sciences Research Council studentshipCambridge Overseas Trust

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Marius Somveille conceived and designed the experiments performed the experimentsanalyzed the data wrote the paper prepared figures andor tables reviewed drafts of thepaper

Somveille et al (2016) PeerJ DOI 107717peerj2658 1522

bull Kate LA Marshall conceived and designed the experiments wrote the paper revieweddrafts of the paperbull Thanh-Lan Gluckman conceived and designed the experiments performed theexperiments wrote the paper prepared figures andor tables reviewed drafts of thepaper

Data AvailabilityThe following information was supplied regarding data availability

We have supplied the raw data used in this analysis for the review process Please donot publish the raw data alongside this article if accepted as a third-party who is not aco-author on this paper partly owns the dataset with T-LG

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj2658supplemental-information

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Troscianko J Lown AE Hughes AE Stevens M 2013 Defeating crypsis detection andlearning of camouflage strategies PLoS ONE 8e73733

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Vignieri SN Larson JG Hoekstra HE 2010 The selective advantage of crypsis in miceEvolution 642153ndash2158 DOI 101111j1558-5646201000976x

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VonHelversen B Schooler LJ Czienskowski U 2013 Are stripes beneficial dazzlecamouflage influences perceived speed and hit rates PLoS ONE 8e61173DOI 101371journalpone0061173

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