the role of tadpole coloration against visually oriented predators

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Behavioral Ecology and Sociobiology ISSN 0340-5443Volume 70Number 2 Behav Ecol Sociobiol (2016) 70:255-267DOI 10.1007/s00265-015-2044-4

The role of tadpole coloration againstvisually oriented predators

Juan Espanha, Marcelo F. de Vasconcelos& Paula C. Eterovick

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ORIGINAL ARTICLE

The role of tadpole coloration against visually oriented predators

Juan Espanha1 & Marcelo F. de Vasconcelos1 & Paula C. Eterovick1

Received: 6 July 2015 /Revised: 15 November 2015 /Accepted: 18 November 2015 /Published online: 28 November 2015# Springer-Verlag Berlin Heidelberg 2015

Abstract An animal’s vulnerability to predators can be influ-enced by its behavior, morphology, body size, coloration, hab-itat preferences, and palatability. We tested whether the color-ation of Bokermannohyla saxicola and Scinax machadoi tad-poles affects their survival when exposed to local visuallyoriented predators at a site in southeastern Brazil. We testedthree aquatic invertebrates (Aeshnidae, Belostoma sp.,Lethocerus sp.) and birds as tadpole predators. We predictedthat predation rates would differ depending on the substratewhere the tadpoles positioned themselves (light or dark), hy-pothesizing that each tadpole would use preferentially a back-ground that conferred camouflage and that predation levelswould be lower on such backgrounds compared to others. B.saxicola had higher survivorship than S. machadoi on light

backgrounds at some instances, in accordance with its crypsishypothesis. However, B. saxicola tadpoles did not use lightbackgrounds more often than dark ones. S. machadoi colora-tion looked disruptive on both light and dark backgrounds,and tadpoles showed no preference or differences in survivalrates between these backgrounds. Predation rates did not differbetween the two species in a way that could confirm a previ-ous hypothesis of aposematic/mimetic coloration for S.machadoi tadpoles. Our results show that colorations that ap-pear to function to impair visual detection may play this role atsome circumstances but not others. Tadpole colorations mayhave evolved in another context, in which avoiding visualdetection by predators was a stronger selective pressure. In acontext with lower predation pressure from visually orientedpredators, the expected background choice behavior for in-creased camouflage may not be strongly selected for.

Keywords Predation .Bokermannohyla saxicola . Scinaxmachadoi . Camouflage . Disruptive coloration . Crypticcoloration . Defensive coloration . Southeastern Brazil

Introduction

Many studies suggest that predation is the major cause oftadpole mortality (Alford 1999), occurring from the egg stage(Villa et al. 1982) until the end of metamorphosis (Wassersugand Sperry 1977; Arnold and Wassersug 1978). The presenceof predators is a limiting factor in the use of ponds by anurans(Woodward 1983; Kats et al. 1988) and may also affect inter-specific interactions in tadpole communities (Morin 1981), forexample, reducing interspecific competition (Herreid andKinney 1966; Calef 1973; Cecil and Just 1979) or affectingtadpole performance and causing size variation (Peacor et al.2007; Costa and Kishida 2015). The main predators of

Behav Ecol Sociobiol (2016) 70:255–267DOI 10.1007/s00265-015-2044-4

Communicated by K. Summers

Significance statement The use of camouflage to avoid visuallyoriented predators may be an effective strategy as long as the prey isable to choose backgrounds that match their body colors (crypsis) ordisrupts identification of body contour by matching some specific partsof the body but not others (disruptive camouflage). We used tadpoles oftwo species to test the hypotheses of (1) effective camouflage reducingpredation and (2) tadpoles choosing backgrounds that promote lowerpredation levels. Although in some circumstances one species was shownto be less predated on a background expected to enhance its camouflage,it did not use this background more often than an alternative. Our resultssuggest that extant predation pressuresmay not be strong enough to shapebackground choice behavior in these tadpoles. Alternatively, tadpolesmay choose backgrounds for camouflage just under imminent predationrisk.

* Paula C. [email protected]

1 Programa de Pós Graduação em Biologia de Vertebrados, PontifíciaUniversidade Católica de Minas Gerais, Belo Horizonte 30535-610,Brazil

Author's personal copy

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tadpoles include some invertebrates such as Belostomatidae(e.g., Lethocerus sp.), Odonata (e.g., Anax sp.), andColeoptera (e.g., Dytiscus sp.; Herreid and Kinney 1966;DeBenedictis 1974; Heyer et al. 1975) and vertebrates suchas fishes, salamanders, newts (e.g., Ambystoma sp.), watersnakes, anurans, and birds (Heyer et al. 1975; Cecil and Just1979; Costa and Kishida 2015).

Tadpole predators use vision to detect their prey in varieddegrees. Belostomatidae often lie motionless at the bottom ofa body of water, attached to various objects, where they waitfor prey to pass by. They then strike, injecting a powerfuldigestive saliva with their rostrum, sucking out the liquefiedremains (Nieser and Melo 1997; Rafael et al. 2012). Althoughthere is no information on how water bugs use their vision forprey detection, some Heteroptera were shown to respond dif-ferently to varied colors based on their wavelength reflection-polarization patterns (Kriska et al. 2006). By hiding amongvegetation, tadpoles can reduce predation risk by water bugs,showing that vision has an important role in prey detection(see Kopp et al. 2006). Odonate larvae are visual and tactilepredators, and their binocular vision aids in estimating thedistance to an object and its size (Corbet 1999). Although theyare specialized to detect movement, odonate naiads are capa-ble of discriminating the shape (Corbet 1999) and color(Pritchard 1965) of immobile prey, with their eyes being sen-sitive to a broad spectrum of wavelengths (Bybee et al. 2012).Many species of dragonfly naiads use visual cues as well astadpole movement and size rather than chemical cues for de-tection (Pritchard 1965; Rebora et al. 2004). Fish, on the otherhand, are more efficient than Odonata in detecting immobileprey visually (Nomura et al. 2011).

Several experiments on predator/prey detection and mor-tality rates have been done involving tadpoles and predatoryarthropods (e.g., Gascon 1992; Takahara et al. 2012; Nomuraet al. 2013) or fish (e.g., Nomura et al. 2011). However, re-ports on tadpole predation by terrestrial vertebrates such asbirds are occasional (e.g., Garwood 2006), with some excep-tions (Sick 1997; Silva and Giaretta 2008).

Differences in the composition of anuran assemblages andtadpole predator communities result in a set of tadpole adap-tations to avoid predation (Woodward 1983; Kats et al. 1988).These include unpalatability (Voris and Bacon 1966;Wassersug 1971), reduction in activity (Caldwell et al. 1980;Woodward 1983; Eklöv and Werner 2000), cryptic coloration(Wassersug 1971), chemical repellents (Voris and Bacon1966; Brodie et al. 1978), changes in activity period (Taylor1983), ability to escape (Werner and McPeek 1994), and abil-ity to seek refuge (Calef 1973).

Tadpoles can benefit from their coloration associated tobehaviors that reduce the risk of detection or predation.Tadpoles of Bokermannohyla alvarengai, for instance, choosebackgrounds that confer improved crypsis when threatened(Eterovick et al. 2010). A cryptic animal resembles random

samples of the habitat background, hampering predator detec-tion (Endler 2006). Disruptive camouflage is also considered aform of effective protection from predators and is character-ized by disruption of the continuity of a surface by a contourof different shape and/or color (Merilaita and Lind 2005).Background color may affect tadpole activity levels in thepresence of predators, with tadpoles being less active on con-trasting backgrounds (Nomura et al. 2013).

Many studies on camouflage and/or its effect on survivalare conducted under controlled laboratory conditions (e.g.,Kjernsmo and Merilaita 2012; Nomura et al. 2013;Dimitrova and Merilaita 2014). Studies under natural condi-tions are more challenging but essential to understand theinterplay between animal color pattern and behavior in pro-ducing camouflage against natural predators (Kang et al.2015). The role of camouflage in increasing survival mustbe associated with appropriate background choice (Kang etal. 2015) and actual decrease in predation rates (Dimitrovaand Merilaita 2014). Tadpoles respond behaviorally to back-ground color (Eterovick et al. 2010; Nomura et al. 2013) andreduce movements when they detect predator presence(Takahara et al. 2012), but the outcome of such responsesagainst different types of predators must be evaluated to un-cover the real role of defensive coloration on survival (Limaand Dill 1990; Nomura et al. 2011; Takahara et al. 2012).

Bokermannohyla saxicola and Scinax machadoi can beabundant as tadpoles in some permanent streams at the mon-tane meadows of the Parque Nacional da Serra do Cipó (Serrado Cipó National Park), and under such circumstances, theyare likely to be an abundant source of food for potential pred-ators. In this case, defensive colorations would be a usefuladaptation to reduce tadpole predation rates. B. saxicola tad-poles are likely to use cryptic coloration as a defense strategy(PCE, personal observation), whereas S. machadoi tadpoleslook disruptive on stream bottom (Eterovick and Sazima2004). Horta et al. (2010), on the other hand, suggested S.machadoi tadpole’s color to be aposematic and possibly mi-metic with a syntopic naucorid (Limnocoris porphyrus, Nieserand Lopez-Ruf 2001; Heteroptera, Naucoridae), although theydid not test this hypothesis. This study aims to investigate withfield experiments the potential defensive role of the colorationof tadpoles of these two anuran species at two streams wherethey are by far the dominant species among local anuran lar-vae. We aimed to investigate the adaptive value of the poten-tially disruptive/aposematic coloration of S. machadoi andcryptic coloration of B. saxicola tadpoles against potentialinvertebrate (Odonata and Belostomatidae) and vertebrate(birds) predators.

We expected tadpoles of B. saxicola to have higher preda-tion rates on dark backgrounds, where they were more visible.These tadpoles have a light hue in the studied streams com-pared to the range of colors observed for the species (PCE,personal observation), thus being very cryptic on light

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backgrounds. We expected tadpoles of S. machadoi not todiffer between light and dark backgrounds considering preda-tion rates if their coloration is disruptive because their lightpatches match light backgrounds and their dark body partsmatch dark backgrounds, interrupting body shape contour inboth backgrounds. We expected them to be more predatedthan B. saxicola on light backgrounds, because although dis-ruptive, they are noticeable whereas B. saxicola can be veryhard to spot in such backgrounds.We also expected them to beless predated than B. saxicola on dark backgrounds, where B.saxicola is more visible/identifiable. On the other hand, weexpected them to be less predated than B. saxicola in all back-grounds if their coloration is aposematic.

Materials and methods

Study system

B. saxicola (Bokermann 1964) occurs mostly at altitudesabove 1,000 m in the Espinhaço mountain range and is en-demic to Brazil and relatively common in its region of occur-rence (IUCN 2012a). It breeds in temporary or permanentstreams with rocky bottom. Males call throughout the yearon rocks by the stream bed. The spawn is a circular clusteradhered to submerged rocks. Brownish tadpoles are mainlynocturnal and remain in backwaters or on rocky bottoms withsome water flow, usually among aquatic vegetation at depthsbetween 5 and 45 cm. Tadpoles are found throughout the yearand larval development lasts at least 5 months (Eterovick andSazima 2004).

S. machadoi (Bokermann and Sazima 1973) belongs to theScinax catharinae species group (sensu Faivovich et al. 2005).S. machadoi can be found in the Espinhaço and MantiqueiraMountain Ranges (IUCN 2012b). It reproduces in permanentstreams with rocky bottom surrounded by riparian forests.Males call during the day and at night, throughout the entireyear (Eterovick and Sazima 2004). Tadpoles are dark with ayellowish patch in front of the eyes and a yellowish spot on thedorsal fin (Bokermann and Sazima 1973). They are activeduring the day and at night, remaining on the bottom at a rangeof depths up to 1.60 m.

The Parque Nacional da Serra do Cipó (19° 12′–19° 20′ S,43° 30′–43° 40′ W) is located at the southern portion of theEspinhaço mountain range inMinas Gerais state, southeasternBrazil. Its higher portions (1,095–1,485 m alt.) are covered bymontane meadow vegetation. The geological formations arequartizitic. The climate shows marked dry (April toSeptember) and wet (October to March) seasons. The parkharbors the headwaters of many rivers from distinct water-sheds and many streams. A total of 42 species of frogs wererecorded at the montane meadows of the Serra do Cipó(Eterovick and Sazima 2004).

We conducted experiments in two third order (sensuStrahler 1957) streams named Água Escura (19° 16′ 02.84″S and 43° 30′ 56.64″W; WGS84, 1,236 m alt.) and Salitreiro(19° 16′ 54.99″ S and 43° 30′ 50.10″ W; WGS84, 1,254 malt.). Both streams have some small falls and rapids (especiallyduring the rainy season) and many backwaters. Their bottomsare covered by a mosaic of whitish pebbles and yellowishrocks or darker sandy or muddy sediment, sometimes withalgae or submerged grasses. Dark debris deposit in rock crev-ices or deeper sections of the bottom. Ours and other researchgroups never observed fishes in the studied streams in manyyears of field work at these specific sites (M. Callisto, personalcommunication).

Based on field observations, we noticed Belostomatidae,Megaloptera, and Odonata to be the biggest and most vora-cious invertebrate predators that could eat tadpoles in the stud-ied streams. Thus, we used two species of Belostomatidae(Lethocerus sp. and Belostoma sp.) and one species ofOdonata (Aeshnidae) as invertebrate predators. The genusLethocerus can reach up to 130 mm in length and includesvoracious ambush predators of crustaceans, fish, and amphib-ians (Rafael et al. 2012; Nieser and Melo 1997). The familyAeshnidae contains the fastest and largest Anisoptera (Rafaelet al. 2012). We chose these species to study because theywere the ones that could be found in large enough numbersto run the experiments in situ. We also expected them to rep-resent the greatest threat to tadpoles locally, due to their abun-dance and predatory habits. Besides the chosen predators, werecorded four other species of Odonata (two Zygoptera andtwo Anisoptera) and two of Megaloptera (Corydalus spp.) butin smaller numbers. There are probably some other aquaticinvertebrates that may prey upon tadpoles in the streams, al-though we did not observe predation events. These areNotonectidae, Corixidae, Naucoridae, and spiders (A. L.Melo, personal communication; Galdean et al. 2000;Galdean et al. 2001; Callisto et al. 2001).

Experimental design—invertebrate predators

Experimental enclosures consisted of transparent plastic box-es (capacity of 29 l; 45.7 cm length, 32.6 cm width, 28.0 cmheight) partially submerged in stream water. We made severalsmall holes (about 3 mm diameter) around the walls of theboxes to allow the water inside the boxes tomix with the wateroutside in order to keep the stream chemical and temperatureextant conditions in the boxes during the experiments. Wecovered the bottoms of the boxes with natural substrata fromthe stream bottom, using rocks as light (yellowish) back-grounds and sand/debris as dark (blackish) backgrounds. Wearranged experimental boxes in backwaters where water flowwas minimal and waited for complete background sedimenta-tion before starting the experiments. Treatments consisted of(1) light, (2) dark, and (3) mixed (half light, half dark)

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backgrounds (Fig. 1a). All treatments had three tadpoles ofeach of the two species (B. saxicola and S. machadoi) andone predator. Controls were identical except for the fact thatno predator was included. Each run of the experimentconsisted of 18 boxes: three replicates of each one of the threetreatments and each one of the three controls. We performedthe experiment with Aeshnidae three times at Água Escurastream (on April, May, and June) and one time at Salitreirostream (on June). We performed the experiment withBelostoma sp. three times at Salitreiro stream (on May, July,and August). We conducted a total of six experiments withLethocerus sp. at Salitreiro stream in June and August 2013(Fig. 1a). Combinations of predator type and stream weredetermined by availability of predators. After the end of eachexperiment, all living animals were returned to the stream. Allexperiments were conducted between April and August 2013.

We captured all tadpoles in situ throughout a 100-m sectionof the stream (what took from 3 to 5 h) and mounted theexperiment right after. We used tadpoles between stages 25and 35 (sensu Gosner 1960) to avoid possible interference oflarge hind limbs on tadpole escape performance. We selectedthe biggest tadpoles of S. machadoi and the smallest tadpolesof B. saxicola to standardize tadpole size between the twospecies. This way we intended to minimize the effect of tad-pole size as an influencing factor on tadpole detection or se-lection by the predator. We kept tadpoles in stream water in-side plastic containers (partially submerged in the stream tomaintain water temperature) until all individuals necessary forthe experiment were collected and then we randomly

distributed them among controls and treatments. We capturedpredators to be used in each experiment at the same night andkept them in individual plastic containers until tadpoles weredistributed among all boxes, then we introduced predators intreatment boxes. We also selected predators within thenarrowest size range possible to minimize potential predatorsize interference on tadpole predation rates/preferences. Wemeasured all predators with calipers (to the nearest 0.1 mm).We checked all the boxes in 24-h intervals (starting the nextday) for 10 days or until one species was eliminated from onebox, whatever happened first. We considered that eliminationof one species would leave no choice of prey to the predator inthat box and thus cause noise in our results. We recorded thenumber of surviving tadpoles by the end of each trial. In ex-periments with Odonata, we noticed that several tadpoles werealive but injured, so we also counted the number of intacttadpoles in these trials. In the experiments with Lethocerussp., we made temporal replicates of treatments and controlsbecause there were not enough predators to conduct spatialreplicates of treatments. Lethocerus spp. were so voraciousthat each run of the experiment lasted a single day, 2 days atmost (when one species was eliminated from one box), and weperformed other two runs alternating predator individualsamong background treatments. Each experiment was consid-ered as three replicate runs of all treatments and controls.

Because natural backgrounds have different textures thatmay influence protection provided to tadpoles (e.g., tadpolesmay be partially hidden under debris but not on rocks), wealso conducted experiments on boxes with the bottoms

Fig. 1 Experimental design usedin tests with invertebratepredators showing treatments,number of tadpoles of eachspecies (B. saxicola and S.machadoi) per experimental box,and number of replicate runs inthe two streams studied: ÁguaEscura (AE) and Salitreiro (Salit.)



painted in yellow, black, and mixed (half yellow, half black;Fig. 1b) to test the effect of color alone on predation rates uponthe two species of tadpoles. Any differences between resultswith natural and painted backgrounds could be interpreted aseffects of properties of natural backgrounds other than color.The boxes were the same, painted outside so that paintchemicals would not interfere on the behavior of experimentalspecies. Experimental design was the same except for theabsence of natural substrate inside the boxes and the use offive tadpoles of each species instead of three (Fig. 1b). Weconducted this experiment twice (on July and August) at ÁguaEscura stream with Aeshnidae as predators and once at eachstream (on September) with Belostoma sp. as predators. Weconducted the experiment four times with Lethocerus sp. aspredator at Salitreiro stream (on September; Fig. 1b).

In order to test for any preference of tadpoles for differentbackgrounds, we conducted experiments to test for back-ground choice using boxes with mixed backgrounds (exactlyas in the mixed background treatment described above;Fig. 2a–d) using both natural and painted backgrounds (asdescribed above). We placed five tadpoles of each species ineach box and recorded the microhabitat they were on 24 hlater to test for preferences (considered as a greater numberof tadpoles on the preferred background—light or dark). Weconducted this experiment with 18 boxes at Água Escura and12 boxes at Salitreiro streams using natural substrata and 18boxes at Água Escura and six boxes at Salitreiro streams withpainted bottoms. The 12 boxes at Salitreiro with natural sub-strata had three tadpoles of each species instead of five.

Experimental design—vertebrate predators

Among vertebrates, birds are the main potential tadpole pred-ators in the studied streams, since fishes are absent. Thus, weconducted experiments to assess the potential adaptive valueof tadpole defensive colors against predatory birds. First, weused transparent plastic trays (25×17×5 cm) with a subdivi-sion (in the middle of their longer axis) forming two compart-ments that we filled with stream water up to about 2 cm. Ineach compartment, we placed one tadpole of each species (B.saxicola and S. machadoi). Trays were placed on the streams,attached to the closest margin by nylon strings, and left float-ing for 24 h, after what we checked them for predated tad-poles. Because B. saxicola tadpoles showed the ability toeventually jump off the trays, we repeated the experiment withfake tadpoles made of non-toxic clay and painted with non-toxic ink. We tested for effects of dark vs. light backgroundsleaving trays over dark stream bottoms and leaving half (20trays) with their transparent bottoms and half (20 trays) over aplastic yellow background (made of the tray’s yellow plasticcover that we placed under its bottom; Fig. 2e, f). We placedtrays in groups of four (two with and two without the yellowbackground).We checked trays every 24 h during 2 to 10 days

at each run of the experiment (we planned to check each run ofthe experiment for 10 days, but some lasted fewer days be-cause of rains that dislodged the trays). Thus, the experimentincluded 40 models (two per tray) of each tadpole species perrun.We conducted this experiment twice at each stream (ÁguaEscura and Salitreiro).

We also conducted visual observations of birds at thestream margins in an attempt to observe events of tadpolepredation (totalling about 440 h of observation distributedfrom 06:00 to 11:00 h and from 15:00 to 18:30 h). At ÁguaEscura, we mounted mist nets crossing the stream to capturepotential species of birds that could be foraging on tadpoles atthe stream. Sampling effort consisted of five to seven mist netsmounted for 3 days at each of three different periods duringthe rainy season (December 2012, January, and February2013) and three during the dry season (July, August, andSeptember 2013), totaling a sample effort of 439 h and40 min (216 h and 30 min on wet season and 223 h and10 min on dry season). The mist nets (2.5 m height, 9 mlength, and 20 mmmesh) were spaced at least 10 m from eachother (20 m at most). Nets were opened in the morning andafternoon and checked every 30 min. We weighed capturedbirds, took measurements, and banded them according toCEMAVE specifications (IBAMA 1994) and then obtainedtheir stomach contents through regurgitation with the use ofemetic tartar according to Sabino and Duca (2011). Weinspected stomach contents in search for tadpole remains.

Third, we conducted some ex situ experiments to test B.saxicola and S. machadoi tadpole palatability for birds anddetectability by birds on light and dark backgrounds. For thispurpose, we used birds maintained in the Centro de TriagemdeAnimais Silvestres (CETAS) aviary in Belo Horizonte City.The center maintains native birds recovered from traffic orcaptivity for recovery and possibly reintroduction. Birds ofseveral species were kept in a common enclosure, Turdusalbicolis Vieillot, 1818, Turdus fumigatus Lichtenstein,1823, Turdus leucomelas Vieillot, 1818, Turdus rufiventrisVieillot, 1818 (Turdidae), and Saltator similis d’Orbigny &Lafresnaye, 1837 (Thraupidae), which are potential tadpolepredators, and also Paroaria dominicana (Linnaeus, 1758)(Thraupidae) and Icterus jamacaii (Gmelin, 1788)(Icteridae). From these, T. fumigatus, P. dominicana, and I.jamacaii do not occur at the study site. All the species wererepresented by two or more individuals in the aviary exceptfor T. leucomelas and I. jamacaii with just one individualeach. We collected tadpoles in the studied streams and tookthem to the CETAS (about 2-h trip in plastic bags with streamwater in styrofoam boxes). We first offered tadpoles (15 ofeach species) in a white tray (40×28×8 cm) filled with streamwater up to 2 cm to the birds in the enclosure to test whetherthey would be willing to feed on the tadpoles and if the tad-poles would be palatable to them. After 30 min, we checkedfor surviving tadpoles. We then offered tadpoles (17 of each



species per tray) in a yellow tray and in a black tray (transpar-ent trays of the same size painted in the outside) to test for anydifferential predation determined by background color. After2 h, we checked for surviving tadpoles. During an attempt toreplicate the experiment with painted trays, the tadpoles acci-dentally died during transportation. Thus, we still conductedthe same experiment but with recently dead tadpoles, whichstill had the same colors. We used nine tadpoles of each spe-cies per tray and checked for non-eaten tadpoles after 1 h. Weadded a wood stick to each experimental tray so that birdscould perch on it to reach tadpoles (which they did). We re-moved the commercial bird food usually offered to the birds atCETAS 1 h before starting each experiment. Blinded methodswere used when all behavioral data were recorded and/or an-alyzed; we established and standardized sampling methodsand statistical procedures a priori to avoid any possible ob-server bias.

Statistical analyses

Because we recorded a single dead tadpole in a control boxduring the whole study, we assumed that mortality recorded intreatments could be considered as the result of predation andthus we did not use data from controls in the analyses. Weused the function glmer in R (R Core Team 2015) to creategeneralized linear mixed models (GLMMs) to test for tadpolesurvival on natural and painted backgrounds separately. Wealso conducted separate analyses for each invertebrate preda-tor tested (Aeshnidae, Belostoma sp., and Lethocerus sp.). Weused tadpole survival (as binary data: 0 for dead, 1 for alive) asthe response variable and background type (light, dark, ormixed) and species (B. saxicola or S. machadoi) as fixed ex-planatory variables. We included replicates of the experimentas random variables: each set of three boxes with one of eachbackground type had a different number, accounting for acombination of possible variations among local replicates,streams, and sampling periods (see Fig. 1 for a summary ofexperimental design). For each analysis, we created a com-plete model including the interaction between backgroundtype and species plus the random variable and compared itto a null model including just the random variable. If thecomplete model presented an increase in fit, we compared itto simpler models (including the two fixed variables withoutthe interaction between them and the random variable andthen including each fixed variable separately with the randomvariable) in order to achieve the simplest model with the bestexplanatory power.

In experiments with Odonata as predator, we conducted anadditional analysis considering tadpole condition (Bdamaged^or Bundamaged^ tadpoles) as the response variable, becausesome surviving tadpoles were injured when exposed to odo-nate predators.

Next, we computed a variable Bdays alive^ for each tadpoleto represent the number of days they survived during the ex-periment (tadpoles that survived until the end of the experi-ment received the number of days that the experiment lasted).Using the same data sets with this additional variable, weanalyzed survivorship using Cox regressions with theBsurvival^ package in R (R Core Team 2015), in an attemptto unveil any difference in survivorship curves between spe-cies and background types that might not be clear from thefinal number of survivors analyzed with GLMMs. We createda survival object and used the interaction between species andbackground types as predictors.We also performed equivalentanalyses to compare Binjury curves^ representing time elapseduntil tadpole injury (instead of death) in experiments withodonate predators that sometimes hurt tadpoles but did notkill them.

In order to test for tadpole background preferences (basedon number of tadpoles on each background color per box), weused the function glmer in R. We built a complete model withthe interaction between species and background as fixed var-iable and experiment (whenever experiments were run two ormore times) and stream (when experiments were conducted inboth streams) as random variables.We then compared it with anull model including only the random variables. We conduct-ed these analyses for experiments conducted at Salitreirousing natural backgrounds and at both streams using paintedbackgrounds. Experiments conducted on natural backgroundsat Água Escura stream had three tadpoles of each speciesinstead of five, so we tested these data separately withMann-Whitney tests because there were no random variablesin this case.

Results

On natural backgrounds, neither background type, tadpolespecies, or their interaction influenced tadpole survivorshipin the presence of odonate predators; the complete modeldid not differ from the null model (chi-square=4.851, df=5,p=0.434; Fig. 3a). The same result applied when we consid-ered, instead of surviving tadpoles, just undamaged tadpolesas those escaping predation (chi-square=3.062, df=5, p=0.690; Fig. 3c). Survivorship curves did not differ amongbackgrounds or species (likelihood ratio test=4.57, df=5, p=0.470). Injury curves did not differ among backgrounds orspecies either (likelihood ratio test=2.55, df=5, p=0.769).

On painted backgrounds, neither background type, tadpolespecies, nor their interaction influenced tadpole survivorshipin the presence of odonate predators at Água Escura stream(chi-square=5.968, df=5, p=0.309; Fig. 3b). Survivorshipcurves did not differ among backgrounds or species either(likelihood ratio test=5.34, df=5, p=0.375). However, con-sidering just undamaged tadpoles as those escaping predation,



the complete model had a marginally significantly better fitthan the null model (chi-square=11.021, df=5, p=0.051;Fig. 3d). A post hoc (Tukey) test showed that damage causedto the two species differed only on light backgrounds, whereS. machadoi tadpoles were attacked in significantly largernumbers than B. saxicola tadpoles; however, the differencewas marginally significant after p value adjustment (singlestep method, p=0.058). The injury curve showed significantlyhigher injury risk for S. machadoi on light backgrounds(likelihood ration test=11.48, df=5, p=0.044; Table 1).

Neither background type, tadpole species, nor their inter-action influenced tadpole survivorship in the presence ofBelostoma sp. on natural (chi-square=7.934, df=5, p=0.160;Fig. 4a) or painted (chi-square=1.096, df=3, p=0.778;Fig. 4b) backgrounds at Salitreiro stream. Survivorship curvesdid not differ either (natural backgrounds: likelihood ratiotest=6.96, df=5, p=0.223; painted backgrounds: likelihoodratio test=1.02, df=3, p=0.796).

For predation by Lethocerus sp. on natural backgrounds,the complete model had the greatest fit and was significantlybetter than the null model (chi-square=20.930, df=5, p=0.001). A model without the interaction between species andbackground also had a significantly better fit than the nullmodel (chi-square=11.508, df=3, p=0.009), as well as a mod-el with just background as fixed variable (chi-square=11.148,

df=2, p=0.004), but not a model with just species as fixedvariable (chi-square=0.361, df=1, p=0.548). A post hoc(Tukey) test for the interaction effect showed that survivorshipof B. saxicola was significantly higher on mixed than darkbackgrounds (p=0.016), and it was also significantly higheron mixed than light backgrounds (p=0.004). Survivorship ofB. saxicola on mixed backgrounds was higher than S.machadoi survivorship on light backgrounds (p=0.033; singlestep method adjusted p values; Fig. 4c). Survivorship curvesalso pointed to higher survivorship on mixed backgrounds(likelihood ratio test=27.61, df=5, p<0.001; Table 1). Onpainted backgrounds, the best model included just back-ground as fixed variable with the best fit compared to the nullmodel (chi-square=11.072, df=2, p=0.004; Fig. 4d). A posthoc (Tukey) test for background showed that tadpoles had asignificantly lower chance of surviving on dark than both light(p<0.001) and mixed (p=0.029) backgrounds. Chances ofsurviving on light and mixed backgrounds did not differ (p=0.328; Fig. 4d). Survivorship curves also pointed to highersurvivorship on light backgrounds (likelihood ratio test=23.01, df=5, p<0.001; Table 1).

When tested for background preference on natural sub-strates, B. saxicola and S. machadoi showed no prefer-ence and did not differ from each other in use of lightor black backgrounds at Salitreiro stream (chi-square=

Fig. 2 Tadpoles of aBokermannohyla saxicola and bScinax machadoi on natural lightbackgrounds at the streambottom, on the transition of lightand dark bottoms in mixed boxesused for experiments withinvertebrate predators (c B.saxicola on light background, andsome dark background can beseen on the top of the picture; d S.machadoi on dark background,and some light background can beseen on the right of the picture)and inside trays used forexperiments with vertebratepredators e with and f without theyellow cover under thetransparent tray (i.e., artificiallycolored backgrounds). Pictures cand d were taken with naturallight and at an appropriatedistance to best show thematching/contrast of tadpolecolors and backgrounds



3.906, df=3, p=0.272; Fig. 5a). At Água Escura stream,B. saxicola used dark backgrounds more often than lightones (U=10.00, df=1, p=0.005), but S. machadoi did notdiffer in use of light and dark backgrounds (U=32.00, df=1, p=0.424; Fig. 5c and Table 1).

On painted backgrounds, B. saxicola or S. machadoi didnot differ in use of light or black backgrounds, neither be-tween them at any particular background, irrespective of ex-periment run or stream (chi-square=2.276, df=3, p=0.517;Fig. 5b and Table 1).

Fig. 3 Proportion of surviving(a, b) and intact (c, d) tadpoles ofBokermannohyla saxicola (graybars) and Scinax machadoi (blackbars) exposed to odonatepredators on natural streambottom backgrounds at bothstreams (a, c) and on paintedbackgrounds (b, d) at ÁguaEscura stream. Light backgroundscorrespond to rocks (a, c) oryellow paint (b, d), and darkbackgrounds correspond tosediments mixed with debris (a,c) or black paint (b, d). Barsrepresent means+SDcorresponding to variabilitybetween streams and amongsampling periods whereapplicable (see Fig. 1 for detailson experiments and replicates)

Table 1 Predictions regarding the potential defensive role of Bokermannohyla saxicola and Scinax machadoi tadpole coloration with testedhypotheses and main results

Prediction Hypotheses Corroborated

B. saxicola cryptic on lightbackgrounds

Greater survivorship of B. saxicola on light/mixedcompared to dark backgrounds

Just for Lethocerus sp. (predator), on natural orpainted backgrounds

Greater survivorship on light backgrounds comparedto S. machadoi

Yes, in experiments with Odonata on paintedbackgrounds (measured by tadpole damage) andLethocerus on natural backgrounds

S. machadoi disruptive onall backgrounds

Equivalent survivorship of S. machadoi in all backgrounds Yes, except for experiment with Lethocerus sp. onpainted backgrounds

Equivalent survivorship of S. machadoi and B. saxicolaon mixed backgrounds

Yes

Lower survivorship of B. saxicola compared to S. machadoion dark backgrounds

No

S. machadoi aposematic Higher predation of B. saxicola compared to S. machadoiin all backgrounds

No

Tadpoles choose background thatpotentially confers camouflage

B. saxicola prefers light backgrounds No

S. machadoi uses both light and dark backgrounds equally Yes



In the experiments with clay tadpoles, we just recorded onepredation attempt on a S. machadoi model that was partiallycut at the base of the tail. The damage could have been doneby a beak. We observed no other models to be missing ordamaged. Even while we were trying to run these experimentswith live tadpoles, we observed no predation after some daysuntil we noticed one tadpole to jump off the tray and thusdiscarded the data.

We captured 35 birds in mist nets representing 15 species, 8families, and 2 orders. From these, eight represented potentialtadpole predators: six T. leucomelas (Turdidae) and twoLochmias nematura (Lichtenstein, 1823) (Furnariidae). Webanded them and obtained their stomach contents. We alsoobtained one additional stomach content from a recapturedL. nematura. The only three other birds that might occasion-ally eat tadpoles were S. similis, Fluvicola nengeta (Linnaeus,1766) (Tyrannidae), and Serpophaga nigricans (Vieillot,1817) (Tyrannidae). No remains of tadpoles or adult frogscould be identified in the stomachs. From these potential tad-pole predators, we observed one species, L. nematura, to for-age frequently in both studied streams. However, we did notobserve any event of tadpole predation by these birds.

In the experiment conducted at CETAS, birds (includingindividuals from all the species in the enclosure but P.dominicana and I. jamacaii) ate 10 tadpoles of S. machadoiand 11 tadpoles of B. saxicola from the white tray. In the

experiment with painted trays, they ate 11 tadpoles from theyellow tray (six S. machadoi and five B. saxicola) and 28tadpoles from the black tray (16 S. machadoi and 12 B.saxicola). In the other run of the experiment with dead tad-poles, they ate 15 tadpoles from each tray (seven S. machadoiand eight B. saxicola from the yellow tray and eight S.machadoi and seven B. saxicola from the black tray).

Discussion

We hypothesized that the colors of B. saxicola and S.machadoi tadpoles might have an adaptive value by increas-ing their chances of survival through hampered detection byvisual predators at their natural habitats. We tested all thepotential visual tadpole predators that occur in large enoughamounts in the studied streams to cause an important selectivepressure. We found evidence that background matching mayincrease tadpole survivorship, at least under some circum-stances. However, there seems to be no strong selective pres-sure to shape tadpole behavior to achieve the best camouflagein all circumstances.

B. saxicola suffered less predation by Lethocerus sp. onlight-painted backgrounds than on dark ones, as well as onmixed natural backgrounds compared to dark ones. Comparedto S. machadoi, B. saxicola tadpoles were indeed preyed

Fig. 4 Proportion of survivingtadpoles of Bokermannohylasaxicola (gray bars) and Scinaxmachadoi (black bars) exposed toBelostoma sp. (a, b) andLethocerus sp. (c, d) on naturalstream bottom backgrounds (a, c)and painted backgrounds (b, d).Experiments were conducted atSalitreiro stream (a–d) and also atÁgua Escura stream for predationby Belostoma sp. on paintedbackgrounds (b). Lightbackgrounds correspond to rocks(a, c) or yellow paint (b, d), anddark backgrounds correspond tosediments mixed with debris (a,c) or black paint (b, d). Barsrepresent means+SDcorresponding to variabilitybetween streams and amongsampling periods whereapplicable (see Fig. 1 for detailson experiments and replicates)



upon/attacked less intensely on light backgrounds under somecircumstances (i.e., by Odonate predators on painted back-grounds and by Lethocerus sp. on natural backgrounds).These results are in accordance with our hypothesis of B.saxicola being cryptic on light backgrounds and, in this case,crypsis would be more effective than S. machadoi tadpole’sdisruptive coloration on light backgrounds (Table 1).However, these results were not consistent throughout all theexperiments. In other instances, we found no difference in B.saxicola and S. machadoi tadpole predation among back-ground types. For instance, predation/attack by Odonata didnot differ between species or among natural backgrounds andpredation by Belostoma sp. did not differ between species oramong natural or painted backgrounds. Predation upon S.machadoi only differed among painted backgrounds in theLethocerus sp. predation experiment, with higher survivor-ship on light or mixed backgrounds compared to dark ones.In the remaining experiments, survivorship did not differamong background types, what is in accordance with ourhypothesis of S. machadoi being disruptive on both lightand dark backgrounds. However, S. machadoi did not sufferless predation than B. saxicola on dark backgrounds as wehypothesized (see Table 1).

Our results indicate that tadpole coloration may play a rolein tadpole survivorship under some but not all circumstances.

On the other hand, tadpole background choice behavior didnot seem to be under strong selective pressure to achieve thepotential camouflage benefits offered by each backgroundtype. We detected background preference in a single instance,when we observed B. saxicola to prefer dark natural back-grounds, where they might have lower survivorship. Thismay be an effect of the amount of fine sediment (decomposingdebris) on dark backgrounds that could confer some protec-tion to tadpoles (although the amount of such sediment in theexperimental boxes was not enough to cover the tadpoles).Maybe the decrease in predation risk does not compensate apossible decrease in the outcome of other activities, such asfood acquisition. Tadpoles may select backgrounds with betterfeeding opportunities despite higher predation risk (Mogali etal. 2015).

Nomura et al. (2013) observed tadpole behavior (move-ment frequency) to change between light and dark back-grounds for Rhinella schneideri (black tadpoles, Bufonidae)and Euphemphix nattereri (light tadpoles, Leiuperidae), al-though predation risk did not differ between these back-grounds. Maybe the use of a more contrasting background iscompensated by decreased tadpole movement rates also in oursystem, what remains to be tested. Increased background com-plexity (i.e., achromatic contrast among background ele-ments) is likely to confer additional protection by increasing

Fig. 5 Proportion of tadpoles ofBokermannohyla saxicola andScinax machadoi using light anddark natural backgrounds inSalitreiro (a) and Água Escura (c)streams and using light- and dark-painted backgrounds (c) in bothstreams combined. Lightbackgrounds correspond to rocks(a, c) or yellow paint (b) and darkbackgrounds correspond tosediments mixed with debris (a,c) or black paint (b). Barsrepresent means+SDcorresponding to variabilitybetween experimental boxes. Allexperiments started with fivetadpoles of each species per box,except for the ones at ÁguaEscura stream naturalbackgrounds (a) that started withthree tadpoles of each species andwas thus analyzed separately



predator search time (Dimitrova and Merilaita 2014); howev-er, Dimitrova and Merilaita (2014) found no experimentalevidence that more complex backgrounds would be more for-giving for imperfect backgroundmatching.Maybe B. saxicoladid not use contrasting dark-painted backgrounds so frequent-ly as they used natural dark backgrounds because they lackedthe natural texture complexity that might give the tadpolessome extra time to escape in case a predator approached. Onthe other hand, tadpoles may only aim their backgroundchoice at improving camouflage when they detect predatorpresence. There are other factors that could have influencedour results such as the mechanisms by which prey use chem-ical and visual cues to avoid predation (Takahara et al. 2012).Tadpoles have evolved multiple complex anti-predator de-fenses, many of which are inducible, such as behavioral, mor-phological, and life historical responses (Werner and Anholt1993; Smith and Van Buskirk 1995). Tadpoles were alsoshown to grow larger and express more extreme defensivephenotypes when exposed to higher predation risk (Costaand Kishida 2015). Thus, the tadpoles of B. saxicola and S.machadoimay not have expressed their whole potential adap-tive background choice behavior in our experimental boxesbecause they contained no invertebrate predators and we be-lieve tadpoles suffer a low (if any) predation pressure by birdsat our studied system.

It is also possible that other tadpole features could affecttadpole performance and complement the efficiency of colorin deterring predation, resulting in similar performances be-tween B. saxicola and S. machadoi. For instance, there is acommon link between morphology and burst speed in tad-poles so that a deep tail and relatively small body increaseburst speed (Dayton et al. 2005). B. saxicola has a strongmuscular tail and actually escapes faster than S. machadoiwhen disturbed (PCE, personal observation). Tadpole adapta-tions against vertebrate and invertebrate predators are likely todiffer. Johnson et al. (2015) showed Lithobates clamitans tad-poles to swim faster and have greater fast-start speed in pondsdominated by fish predators compared to those dominated byinvertebrate predators. Other studies showed that tail lures(including contrasting marks and medially deep tail fins)may be selected for under high predation pressure by inverte-brates (Van Buskirk 2002; Relyea 2004). Behavior is also animportant anti-predator adaptation (Skelly 1994). Nomura etal. (2011) suggests that the anti-predator traits of tadpoles caninteract with each other, with cryptic tadpoles showing lessermortality when co-occurring with unpalatable tadpoles andodonate predators. However, this is not the case in the presentstudy. Although it has been hypothesized that S. machadoitadpoles might be aposematic (Horta et al. 2010), they areactually palatable to all predators tested (Odonata,Belostomatidae, and birds).

Althoughwe failed to observe tadpole predation by birds inthe studied streams, the experiment conducted at CETAS

proved both B. saxicola and S. machadoi to be palatable toseveral species of birds that would be willing to feed on tad-poles. Although bird diets are important components of birdecology, related knowledge is still incipient for the richBrazilian avifauna (e.g., Manhães 2003; Lopes et al. 2005a;Lima et al. 2010), so reports on tadpole ingestion are mostlyanedoctal. Tadpole predation by birds is hard to observe in thefield, and we expect it to be hard to detect tadpole remains inbird stomachs, since their soft bodies are likely to be promptlydigested (although there is no available information for thestudied species). However, if the studied tadpoles were a con-stant item in the diet of any local bird species, we believe oursampling effort would have been enough to at least detect andconfirm predation by birds in the study system. That did nothappen, indicating that bird predation pressure on tadpoles ofthe two studied species might be, at most, occasional.

Lopes et al. (2005b) investigated whether passerine birdsact as important predators of small vertebrates within theNeotropics by surveying published studies on bird diets, andinformation on labels of museum specimens, compiling dataon the contents of 5,221 stomachs. Eighteen samples (0.3 %)presented evidence of predation on vertebrates. Their datasuggest that vertebrate predation by passerines is relativelyuncommon in the Neotropics and not characteristic of anyfamily. On the other hand, although rare, the ability to preyon vertebrates seems to be widely distributed amongNeotropical passerines, which may respond opportunisticallyto the stimulus of a potential food item.

In conclusion, the colors of B. saxicola and S. machadoitadpoles do not seem to consistently improve survivorship onbackgrounds that increase their cryptic or disruptive potential.Invertebrate predators that are likely to offer the greatest pres-sure in the studied streams ate S. machadoi in larger amountsthan B. saxicola on light backgrounds in some instances butnot in others. Besides, tadpoles of B. saxicola that are expect-ed to suffer less predation on light backgrounds showed nobackground preference that could be attributable to an attemptto improve crypsis potential. Birds seem to be occasional tad-pole predators at the study site, and even if they do prey upontadpoles, ex situ experiments indicated that they would alsoprey indiscriminately upon both B. saxicola and S. machadoion both light and dark backgrounds. Tadpole color may haveresulted from past selective pressures and could have evolvedin a different context in which avoiding visual detection bypredators was a stronger selective pressure. It is also possiblethat current tadpole color is plesiomorphic and was not direct-ly selected for. They may be a by-product of evolution guidedby selection of other features. Otherwise, they may aid toimprove tadpole survival in combination with other strategieslike predator detection ability, control of movement rate, andescape speed. Tadpoles may choose and balance their defen-sive strategies according to extant risk, physiological needs,and opportunities. Studies like the present one are important to



show that not everything that looks adaptive actually is. Theexpected outcomes of a potentially adaptive trait must be test-ed before it is considered as an adaptation to a given function.Our results showed that colorations that appear to function toimpair visual detection may actually not play this role in aconsistent way, at least in the present context.

Acknowledgments We are thankful to J. Kloh, H. Kiefer, L. Penna, G.Pimenta, E. Souza, F. Cristóvão, and others for help during field work, toJ. E. C. Figueira, L. Schiesari, and two anonymous referees for sugges-tions on previous versions of this manuscript, to F. S. Neves, A. Viana,and C. A. Galdino for help with statistics, to CEMAVE and Sisbio/ICMBio for permits (35152-1), to Fundação de Amparo à Pesquisa doEstado de Minas Gerais (Fapemig; CRA APQ 01274-13), and toConselho Nacional de Desenvolvimento Científico e Tecnológico(CNPq) for the scholarships provided to JEMD and PCE (ProductivityGrant 304422/2014-2).

Compliance with ethical standards

Funding This study was funded by Fundação deAmparo à Pesquisa doEstado de Minas Gerais (Fapemig; CRA APQ 01274-13) and ConselhoNacional de Desenvolvimento Científico e Tecnológico (CNPq) whoprovided scholarships to JEMD and PCE (Productivity Grant 304422/2014-2).

Conflict of interest The authors declare that they have no competinginterests.

Ethical approval All applicable international, national, and/or institu-tional guidelines for the care and use of animals were followed (permitobtained from ICMBio/Sisbio: 35152-1). During the whole study, 122 B.saxicola tadpoles and 126 S. machadoi tadpoles were predated, and 25and 47 tadpoles, respectively, were injured by predators. This article doesnot contain any studies with human participants performed by any of theauthors.

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the role of tadpole coloration against visually oriented predators

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