Zoology 129 (2018) 45–53

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Zoology

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Ontogenetic Changes in the Diet and Head Morphology of an Omnivorous Tropidurid ( thoracicus) T ⁎ Ken S. Toyamaa,b, , Karina Junesb, Jorge Ruizb, Alejandro Mendozab, Jose M. Pérezb a Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, M5S 3B2, Canada b Laboratorio de Estudios en Biodiversidad (LEB), Universidad Peruana Cayetano Heredia, Av. Honorio Delgado 430, Urb. Ingeniería, S.M.P., Lima, Peru

ARTICLE INFO ABSTRACT

Keywords: Ontogenetic shifts from an insectivorous diet towards an herbivorous one are well known in . Energetic, head shape behavioral and morphological factors have been linked to this pattern, but the latter have received less attention, herbivory especially with respect to head morphology. It is known that robust heads are related to stronger bite forces, functional morphology consequently facilitating the consumption of harder or tougher, more fibrous items such as plants. In this study ontogeny the ontogeny of diet and head morphology of the omnivorous tropidurid lizard Microlophus thoracicus are de- trophic niche scribed. We found a significant ontogenetic shift from a mainly insectivorous diet in juveniles to a mainly herbivorous one in adults. In parallel, we measured the length, height and width of the head of the studied individuals. We found that adult individuals showed proportionally taller and wider heads when compared to juveniles, and that these increases in proportional head dimensions were significantly correlated with the in- crease in plant material in the diet that we observed. Additionally, we compared the morphologies of adults and juveniles of M. thoracicus and two other Microlophus species known to be insectivorous. These comparisons showed that M. thoracicus adults have proportionally more robust heads when compared to their insectivorous congeners, which is in agreement with the hypothesized link between head morphology and diet characteristics. The results of this study suggest that the known relationship between herbivory and head morphology is maintained even in an ontogenetic context, but further study is needed to determine the effect of other selective pressures which influence these changes in morphology.

1. Introduction with age (Valverde, 1967; Fleet and Fitch, 1974; Ballinger et al., 1977; Van Devender, 1982; Rocha, 1998; Durtsche, 2000; Fialho et al., 2000). Diet is one of the primary features that define an organism's eco- Insects are diet items that contain high amounts of energy; thus, one logical niche (Pianka, 1973) and has been widely studied in lizards explanation for this pattern is that juveniles need a higher rate of en- (Pough, 1973; Pianka, 1986; Losos and Greene, 1988). Most lizards are ergy acquisition to promote rapid growth and thereby reduce their insectivorous; however, some species are omnivorous or even entirely predation risk (Durtsche, 2000). From an energetic point of view, herbivorous. Herbivory is rare among as only around 2% of Pough (1973) similarly suggested that lizards of smaller size would squamate species exclusively consume plants (Cooper and Vitt, 2002; have higher energy requirements per unit of body weight than lizards Espinoza et al., 2004). The evolution of plant consumption in lizards with larger bodies, making insects more profitable than plants for ju- has been related to the efficiency of energy acquisition, reduced inter- veniles because of their high energy content. In contrast, the larger specific competition, resource availability, insularity and foraging adult individuals should benefit from a diet based on plant material, mode (Pough, 1973; Rand, 1978; Pérez-Mellado and Corti, 1993; Van which is readily available in the environment and requires less energy Damme, 1999; Cooper and Vitt, 2002), but other factors, like phylo- to collect than an equivalent volume of energy from insect sources. genetic constraints and climate, have also been shown to be relevant Plant material requires more intensive digestive processes when (Espinoza et al., 2004). compared to other types of items, and its consumption has promoted Ontogenetic changes in diet have been observed previously in om- special adaptations in lizards like microbial fermentation (Troyer, nivorous lizards. Typically, in such species, juveniles are mainly in- 1991; Bjorndal, 1997; Kohl et al., 2016) and morphological features sectivorous and the proportion of plant material in their diets increases related to the digestive tract (Troyer, 1991; O’Grady et al., 2005; Herrel

⁎ Corresponding author: Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street 3041, Toronto, Ontario, M5S 3B2, Canada. E-mail address: [email protected] (K.S. Toyama). https://doi.org/10.1016/j.zool.2018.06.004 Received 24 January 2018; Received in revised form 14 June 2018; Accepted 18 June 2018 Available online 19 June 2018 0944-2006/ © 2018 Elsevier GmbH. All rights reserved. K.S. Toyama et al. Zoology 129 (2018) 45–53 et al., 2008). Further, a plant-based diet has also been shown to shape 17:00 h each day, and the captured individuals were euthanized and head morphology (Herrel et al., 2004; Herrel, 2007). Lizard head shape immediately dissected following standardized procedures (Pisani, 1973; can be related to diet via the impact of shape on bite performance Pérez et al., 2015). The digestive tract components, as well as other (Herrel et al., 2001a,b; McBrayer, 2004). Theoretically, a stronger bite internal organs, were preserved separately in ethanol (70%). The col- force allows lizards to consume harder prey (Herrel et al., 2001a,b; lection of these specimens was performed as part of a larger project Verwaijen et al., 2002; Herrel, 2007; Huyghe et al., 2009), like certain involving endoparasitism in coastal Peruvian lizards. Juveniles were types of insects (Herrel et al., 1998; Miles et al., 2007). Moreover, given separated from adults; a specimen was considered to be a juvenile if its the difficulties of processing their tough and fibrous materials, plants SVL was below 55 mm following Dixon and Wright (1975). Using these are also included among the dietary items that are related to stronger criteria, we assembled a sample of 33 juveniles and 55 adults (29 fe- bite forces (Herrel, 2007; Pietczak and Vieira, 2017). Taller and wider males and 26 males). heads are expected to produce stronger bite forces, this being a pattern that has been observed in multiple independent groups of lizards and is considered to be robust (Herrel et al., 2001a,b; Miles et al., 2007; 2.1. Diet McBrayer and Corbin, 2007; Dollion et al., 2017). Consequently, tall and wide heads are already considered as characteristics of herbivorous Twelve of the 88 collected individuals presented empty or near- lizards (Herrel, 2007). empty stomachs and were not considered in the diet analysis. The In this study we describe the diet and head morphology of contents of the 76 stomachs from the remaining individuals (32 juve- Microlophus thoracicus (Tschudi, 1845), a tropidurid lizard species niles and 44 adults) were analyzed using a stereomicroscope. A pre- found along the deserts of western Peru. Some existing studies have vious study in M. thoracicus found that a minimum of 16 individuals described the diet of this species and found that plant material is an would make an adequate representative sample of the diet character- important component of it (Pérez and Balta, 2007; Pérez et al., 2015). istics of the species (Pérez et al., 2015), thus supporting that the sample However, no studies have conducted an ontogenetic examination of the size used in this study is adequate for diet analyses. Arthropods were diet or morphology of M. thoracicus or any species of Microlophus. Even identified to the Order level and to Family in the case of ants (For- though a previous study did not find differences between the diets of micidae). All plant components were classified into the following ca- juveniles and adults of M. thoracicus (Pérez et al., 2015) we hypothe- tegories: leaves, seeds or flowers. The number and volume of each type size, based on personal observations, that an increased sample effort of item was registered for each individual. The following ellipsoid will allow us to identify an ontogenetic change in a diet initially com- formula was used to estimate the volume of each type of dietary item: posed mainly by insects towards one based mainly on plant material. This expectation is based on what has been observed in other species of 4 LA2 omnivorous lizards (Fleet and Fitch, 1974; Ballinger et al., 1977; Van π ××⎛ ⎞ 322 Devender, 1982; Rocha, 1998; Fialho et al., 2000; Maia-Carneiro et al., ⎝ ⎠ 2017). Additionally, we predict that an ontogenetic change in diet will where L is the length of the ellipse and A, the width (Durtsche, 2000). In also imply a change in some morphological proportions of the head that the case of plant items, all the material belonging to the same category could facilitate stronger bite forces, allowing the adult individuals to (leaves, flowers or seeds) found in a stomach was gathered together and eat plant material. a single volume measurement was calculated. The number and volume Previous studies have shown that differences in head dimensions are of each item type were summed for each age group (adults and juve- related to differences in diet among species of the genus Microlophus niles) and for all the individuals as a group (juveniles + adults). Ad- (Toyama, 2016) and have also suggested that head morphology might ditionally, the frequency of each item in the diet was measured within be evolutionarily labile in respect to ecological factors in several species each group by counting the times at least one dietary item of a given of tropidurine lizards when compared to other morphological traits type appeared in an individual stomach. Posteriorly, an importance (Kohlsdorf et al., 2008; Toyama, 2017). Taking this into account, we index (I ) was calculated considering these three variables (number, aim to describe the ontogeny of the diet and head morphology of M. x frequency and volume) for each of the determined groups (see Powell thoracicus, and to test for correlations in the characteristics of both et al., 1990; Pérez et al., 2015; Zamora-Abrego and Ortega-León, 2016): variables. We are aware that the ontogeny of head morphology can be affected by other natural history characteristics besides diet, like an- I tagonistic interactions between adult individuals (e.g. Lailvaux, 2004). x=+ (% of Number % of Frequency + % of Volume)/3 Considering this, we also compare the head morphology of M. thor- acicus with that of other two Microlophus species known to be pre- Additionally, trophic niche amplitude was estimated using dominantly insectivorous: M. peruvianus and M. occipitalis. We predict Simpson's index (Simpson, 1949; Krebs, 1999): that adult M. thoracicus will show different head characteristics (i.e., 2 Bij =1/Σpi wider and taller heads) when compared to the other two species be- cause of their divergent diet. In contrast, we expect juvenile M. thor- where p is the proportion of the ith item type in the diet. Pianka's index acicus to show a head morphology similar to that of the other two (Pianka, 1974) was also calculated to assess the level of overlap be- species, as their diets would be also similar (i.e., mainly insectivorous). tween the diets of juveniles and adults. The following formula was used: O =Σp p /(Σp 2 Σp 2)1/2 2. Material and methods jk ij ik ij ik where i is a given type of item and j and k would be, in this case, the Eighty-eight M. thoracicus individuals were sampled in October of different age groups. The output of this index is a number between zero 2012 through visual encounter surveys along a continuous transect (absence of overlap) and one (complete overlap), being values of 0.60 between two localities in the deserts of Ica, Peru: Guadalupe and above considered to indicate a high overlap (Pérez and Balta, (13º59'22.6"S, 75º45'13.1"W) and Huarangal (14º12'42.36"S, 2007). The proportions for each item for these indexes were based on 75º27'41.64"W), which correspond to the Sechura desert ecoregion volumetric proportions and were arcsin-transformed prior to analyses. (Olson et al., 2001). The landscape of the sampling area was always A linear regression between proportion of plant material in the diet and dominated by dispersed patches of Prosopis sp. trees or bushes, and SVL was performed to assess how the presence of this item changed small to medium sized rocks were also common, but dispersed. The with age. A t-test was used to compare the mean proportion of plant captures were performed by hand, approximately between 10:00 and material in the diet between juveniles and adults.

46 K.S. Toyama et al. Zoology 129 (2018) 45–53

2.2. Head morphology The Simpson index for adults was 3.16. Considering all the individuals of the species together we obtained that the main dietary items in terms Besides SVL, three morphological traits were measured: head length of number were insects of the order Diptera (40.55%); in terms of vo- (HL, measured from the tip of the snout to the line formed by the jaw lume, leaves (45.93%), and in terms of frequency, insects of the order junctions), head width (HW, the widest part of the head behind the Coleoptera (84.21%). The importance index indicated that the most eyes) and head height (HH, the distance between the bottom of the important items in the diet of the species as a whole were leaves head and the highest part of the head along the midline). All mea- (44.25), coleopterans (34.36) and dipterans (28.40). The overall surements were taken manually with a digital caliper (0.01 mm preci- Simpson index was 3.58. The Pianka index for niche overlapping be- sion) and log-transformed prior to analysis. tween juveniles and adults was 0.711, a value indicating a high level of To examine possible differences between age groups and sexes in overlap. respect to individual head dimensions we performed analyses of var- When we compared the diets of juveniles and adults, we found that iance on the three head traits with sex and age as factors and with SVL the consumption of plant material by volume proportion was sig- as a covariate. We also assessed head shape by performing analyses of nificantly different between these two groups (t-test, t = -4.346, variance on HW and HH that used HL as the covariate instead of SVL; p < 0.001). The number, volume and frequency of plant components these analyses also incorporated sex and age as factors. In the cases significantly increased in the diet from the juvenile to the adult stage where significantly different slopes would not allow comparisons be- (Fig. 1,R2 = 0.254, p < 0.001; Table 1). tween groups we applied the Johnson-Neyman (JN) technique to de- termine regions of non-significance between groups along the range of 3.2. Morphology the covariate (Johnson and Neyman, 1936; White, 2003). Finally, to determine the degree of association between morphological character- The average snout-vent length (SVL) of the examined individuals of istics and herbivorous diet, a two-block partial least-squares analysis the species M. thoracicus was 58.56 mm ( ± 15.93, n = 88), with values was performed (Adams and Rohlf, 2000). HL, HW and HH were the ranging from 30.3 to 86.8 mm. morphological variables considered while diet was represented by the No differences were detected in the relationships between HL and proportion of seeds, flowers and leaves. The significance of the asso- SVL between juveniles and adults (Table 2, Fig. 2A). The relationships ciation between these variables was assessed through permutation tests. between HW and SVL showed different slopes for adults and juveniles, but the body size region of non-significance was situated in adult sizes, 2.3. Morphological comparisons with other Microlophus species indicating that the higher adult slope does not produce significant differences when compared to juveniles (Tables 2 and 5; Fig. 2B). Ju- To compare the head dimensions of M. thoracicus with other closely veniles exhibited taller heads than adults for a given SVL (Table 2, related taxa we examined preserved specimens from other two species: Fig. 2C). M. occipitalis (n = 77, SVL = 26.9 – 69.8 mm) and M. peruvianus When HL acted as a covariate, regions of non-significance were (n = 49, SVL = 46.2 – 110.7 mm). Although preservation can affect calculated for all cases (Fig. 3), since the differences between the slopes morphological dimensions in museum specimens this issue would only of different groups were always significant or close to significance be relevant when comparing individuals within populations (Vervust (Table 3). The results show that, for a given head length, adults have et al., 2009). Moreover, head traits are among the features that are less wider and taller heads when compared to juveniles (Tables 3 and 5; affected by preservation (Vervust et al., 2009) making it unlikely to Fig. 3A, B). significantly affect our results. For these analyses, adults and juveniles For the following comparisons between sexes only adults were of M. thoracicus were considered as separate groups. We performed considered. No differences were found between the sexes in the length analyses of variance on the three head traits with SVL as a covariate, and width of the head for a given SVL (Table 2; Fig. 2D, E). However, and on HW and HH with HL as a covariate. Species was considered as a males presented significantly taller heads when compared to females factor for both analyses, juveniles and adults being separated in the case (Table 2, Fig. 2F). For a given HL males presented wider and taller of M. thoracicus. The JN method was again used in cases where the heads than females (Table 3, Fig. 3C, D). assumption of slope homogeneity was not met; otherwise post-hoc A significant association between morphology and herbivory was Tukey HSD tests were used for comparisons between groups. Because found by the two-block partial least-squares analysis (r = 0.5075, the two added species are mainly insectivorous in all their life stages we prand < 0.001) with the three head traits loading strongly with the expected differences in head dimensions related to herbivory (i.e. HW morphology axis (correlation coefficients; HL = 0.957, HW = 0.987, and HH) between them and adult M. thoracicus individuals. These and HH = 0.980) and leaves loading strongly with the diet axis (correlation the previous analyses were performed in R (R Core Team, 2016). coefficients; leaves = 0.776, flowers = 0.253, seeds = -0.269).

3. Results 3.3. Comparisons between species

3.1. Diet For the following comparisons between species, M. thoracicus in- dividuals were categorized as adults or juveniles and considered as A full characterization of the diet of M. thoracicus is shown in separate groups. All the interspecific analyses revealed that groups Table 1. For juveniles, the most important dietary items in terms of differ in the slopes and intercepts of their allometric relationships number were the insects of the order Diptera (58.89%); in terms of (Table 4). Pairwise comparisons were performed when possible, and volume, insects of the order Coleoptera (21.79%), and in terms of fre- non-significance regions were calculated when necessary (Table 5). quency, insects of the family Formicidae (96.88%). The Importance For a given SVL both groups of M. thoracicus, and M. occipitalis did Index (Ix) indicated that dipterans (47.55), followed by coleopterans not show differences in HL. When compared to these three groups, M. (40.54) and leaves (35.89) were the most important components of the peruvianus showed longer and shorter heads but only on the larger and diet of M. thoracicus juveniles. The Simpson index for juveniles was smaller extremes of its range size respectively (Fig. 4A, Table 5). With 6.69. In M. thoracicus adults, in terms of number the most important respect to HW, adults and juveniles of M. thoracicus did not show dif- items were flowers (36.08%); in volume, leaves (49.94%), and in fre- ferences between them for a given SVL and both groups showed wider quency, insects of the order Coleoptera (77.27%). The Importance heads than M. occipitalis and M. peruvianus (Fig. 4B, Table 5). Across Index showed that the most important dietary items for adults were most of its size range, M. peruvianus presents wider heads than M. oc- leaves (46.62), followed by flowers (34.36) and coleopterans (31.95). cipitalis (Fig. 4B, Table 5). With respect to HH, juvenile M. thoracicus

47 K.S. Toyama et al. Zoology 129 (2018) 45–53 – V (%) F F (%) Ix = importance index (see methods section for the (%) V x Fig. 1. Plant material consumption in M. thoracicus. Arcsin-transformed pro- portions of plant material (volume of all the plant components together) in the diet of M. thoracicus in respect to the snout-vent length (log-SVL). The solid line 2 Total (n = 76) 1413 100 23108.1 100 76 nn represents the regression between both variables, n = 76, R = 0.254, t = 5.148, p < 0.001. ), F = frequency, I 526.8––– 2.28 24 31.58

3 presented taller heads than adult M. thoracicus and M. peruvianus, but differences with M. occipitalis were not significant in an important re- gion of their size ranges (Fig. 4C, Table 5). Adult M. thoracicus showed taller heads than M. peruvianus and M. occipitalis. Finally, M. peruvianus presented taller heads than M. occipitalis (Fig. 4C, Table 5). The following comparisons considered HL as a covariate. With re- spect to HW, adult M. thoracicus showed wider heads than the re- maining groups. Juvenile M. thoracicus presented wider heads than M. V (%) F F (%) Ix occipitalis but no differences were found when compared to M. per- uvianus. M. peruvianus presented wider heads than M. occipitalis (Fig. 5A, Table 5). With respect to HH, adult M. thoracicus showed taller heads than all the remaining groups. M. peruvianus presented taller heads than M. occipitalis and juvenile M. thoracicus but this latter dif- ference was not significant at larger sizes. Juvenile M. thoracicus pre- (%) V sented taller heads than M. occipitalis (Fig. 5B, Table 5). Adults (n = 44) nn 474 100 20336.4 100 44 4. Discussion

The results confirmed the substantial presence of plant material in

441.4––– 2.17 10 22.73 the diet of M. thoracicus and the hypothesized differences between ju- veniles and adults with respect to the consumption of this resource. The difference in the diet composition of both groups was evident in terms of the number, volume and frequency of plant material consumed (Table 1), and an ontogenetic progressive change was observed in re- spect to all the plant material in the diet (Fig. 1). However, some si- milarities were observed between the diets of the different age groups. For example, coleopterans were an important food source in the diets of both age groups, and plant components were also ingested by juveniles and adults. This finding is supported by previous studies that examined the diet of this species (Pérez and Balta, 2007; Pérez et al., 2015). 85.4 3.08 14 43.75 Simpson's index was different between both groups (juveniles: 6.69, adults: 3.16). Higher index values indicate a greater diversity of prey

(%) V V (%) F F (%) Ix items, juveniles thus exhibited a higher diversity of dietary items when compared to adults. This could be explained by the inclusion of rela- tively important quantities of plant material in the juvenile diet without 27 2.88 57 2.06 14 43.75 16.23 29 6.12 652 3.21 8 18.18 9.17 56 3.96 709 3.07 22 28.95 11.99 Juveniles (n = 32) 5722 6.07 2.3419 604 39 2.02 21.79 1710 1.41 30 1.06 93.75 0.61 18 4 40.54 56.25 16 36 20.00 50.00 0.14 14 7.59 17.55 8 2.95 13 2232 25.00 57 2.74 10.98 8.74 70 34 4 0.28 77.27 0.34 10 31.95 0.84 22.73 93 8 16 8.65 18.18 6.58 36 7.09 0.08 2836 2.55 32 4 12.27 96 9.09 2.26 64 3.34 84.21 87 0.42 34.36 14 28 0.38 0.99 36.84 24 20 13.27 31.58 11.41 0.09 12 15.79 5.62 nn 34 3.62 89553 58.89 3.21 41649 28 15.01 5.2264 87.5022 22 52.7 6.822 31.44 68.75 2.34 10 456.6 1.90 0.21 47.55 565 2.11 16.47 20 225 26 27 20.38 247 81.25 4.22 8.12 84.38 4 29.46 173 35.89 1.21 2 29 12.50 103 11.74 10 6.25 0.85 6.12 21.73 171 22.73 4.86 1691 10 10157 36.08 8.68 22.73 1 4384 49.94 8.32 44 9.27 30 0.21 22 21.56 573 3.11 68.18 50.00 112 20 40.55 336 46.62 21.48 45.45 589 167 0.55 78 34.36 1.45 11.82 193 1 2.55 5.52 38 10613.6 13.66 2.27 1743.7 32 50.00 45.93 4949 42.11 1.01 18.19 57 7.55 28.40 75.00 3 21.42 48 44.25 24 63.16 0.21 31.58 25.41 337 22.22 1.46 3 3.95 1.87 –– 939 100 2771.7 100 32

. Separate values are shown for juveniles, adults and all the individuals together. n = number, V = volume (mm decreasing the relative importance of arthropods. In the case of adults, similar values for trophic niche amplitude have been found for other Microlophus species (Pérez and Balta, 2007; Quispitúpac and Pérez, 2009) suggesting a trend of trophic niche reduction in adults within this genus. These patterns could be explained by the displacement of juve- niles by adults to sub-optimal habitats, as has been shown in other li- ed fi zard species (Delaney and Warner, 2016, 2017). Juveniles’ inability to Microlophus thoracicus access the main dietary component of the adults (plant material in this study), would force them to expand their dietary preferences. Item Araneae Coccinelidae larvae Coleoptera Hymenoptera Diptera Hemiptera Hymenoptera (Formicidae)Hymenoptera (other) 58Larvae Lepidoptera 6.18Leaves 22Flowers 122Seeds 2.34Not identi 4.40 39 31 1.41 96.88 35.82 18 30 56.25 20.00 6.33 14 47 2.95 57 0.23 24 0.28 54.55 20.37 10 88 22.73 8.65 6.23 36 169 2.55 0.73 96 55 72.37 0.42 26.44 28 36.84 13.27 Total ’ Table 1 Diet of explanation of each variable). A value of 0.71 was obtained for Pianka s overlap index, which

48 K.S. Toyama et al. Zoology 129 (2018) 45–53

Table 2 ANCOVA results for comparisons of head length, width and height between adults and juveniles (Age, top part of the table) and between males and females (Sex, bottom part of the table) with SVL as a covariate. Comparisons between sexes were performed only on adults. Significant p-values are showed in bold.

log(HL) log(HW) log(HH)

F p F p F p

log(SVL) 459.828 < 0.001 2735.173 < 0.001 1960.025 < 0.001 Age 0.065 0.779 3.582 0.062 4.864 0.03 log(SVL) × age 0.392 0.533 7.107 0.009 0.117 0.733 log(SVL) (only adults) 51.095 < 0.001 528.388 < 0.001 253.202 < 0.001 Sex 0.483 0.49 1.379 0.246 6.056 0.017 log(SVL) × sex 0.788 0.379 0.052 0.821 0.838 0.364

suggests that there is a relatively high degree of diet overlap between 2001b; Herrel, 2007). At an intraspecific level, when removing the ef- juveniles and adults (Pérez and Balta, 2007). This degree of overlap in fect of SVL, we found no differences between juveniles and adults in the diets is probably due to the sharing of some important dietary items respect to HL and HW, but juveniles showed taller heads than adults for between juveniles and adults (e.g. coleopterans, ants) in spite of the diet a given body size, suggesting a decrease in the growth rate of this head shift and different trophic diversity indexes already described. dimension with age (Fig. 2A–C). However, when analyzing the shape of We found these important changes in diet to be in agreement with the head adults showed wider and taller heads than juveniles when the patterns observed in head morphology, in accordance with what has removing the effect of HL (Fig. 3A and B). This indicated that the ro- been reported for diet ecomorphology studies in the past (Herrel et al., bustness of the head increases with age, ultimately favoring the

Fig. 2. Allometric relationships between head traits and SVL in M. thoracicus. From A to C all the individuals in the study are shown (Adults: n = 55; R2 for HL = 0.485, HW = 0.908, HH = 0.810; all p < 0.001. Juveniles: n = 33; R2 for HL = 0.716, HW = 0.895, HH = 0.920; all p < 0.001). D to F show relationships for adult individuals (Males: n = 26; R2 for HL = 0.410, HW = 0.851, HH = 0.786; all p < 0.001. Females: n = 29, R2 for HL = 0.298, HW = 0.852, HH = 0.591; all p < 0.005). Comparisons were done based on the logarithm transformation of head traits and SVL. Grey region in B represents the non-significance zone determined by the JN method. Legend shown in figure.

49 K.S. Toyama et al. Zoology 129 (2018) 45–53

Fig. 3. Allometric relationships of head width and height versus head length in M. thoracicus. In A and B all the individuals are shown (Adults: n = 55; R2 for HW = 0.541, HH = 0.318; all p < 0.001. Juveniles: n = 33; R2 for HW = 0.784, HH = 0.60; all p < 0.001). C and D show relationships for adult individuals (Males: n = 26; R2 for HW = 0.453, HH = 0.284; all p < 0.005. Females: n = 29, R2 for HW = 0.393, p < 0.001; R2 for HH = 0.050, p = 0.128). Comparisons were done based on the logarithm transformation of head traits and SVL. Grey areas represent non-significance zones determined by the JN method. Legend shown in figure.

Table 3 in lizards and is considered to be related to antagonistic interactions ANCOVA results for comparisons of head width and height between adults and between males, especially in territorial species (Huyghe et al., 2005; juveniles (Age, top part of the table) and between males and females (Sex, Lappin et al., 2006; Donihue et al., 2015). These proportionally smaller bottom part of the table) with head length as a covariate. Comparisons between head dimensions, however, would not impede females from having a fi sexes were performed only in adults. Signi cant p-values are showed in bold. plant-rich diet, as most of them showed plant material percentages log(HW) log(HH) higher than 80% in their diet (results not shown). Moreover, comparisons between species showed that, when we re- F p F p moved the effect of body size, M. thoracicus had proportionally wider

log(HL) 705.592 < 0.001 390.36 < 0.001 and taller heads than its congeners, which are mainly insectivorous Age 20.183 < 0.001 20.4 < 0.001 (Dixon and Wright, 1975; Pérez and Balta, 2007; Quispitúpac and log(HL) × age 3.817 0.054 6.26 0.0143 Pérez, 2009). Since M. thoracicus and M. peruvianus are closely related, log(HL) (only adults) 82.68 < 0.001 37.95 < 0.001 and both belong to a different clade than M. occipitalis (Benavides et al., Sex 13.65 < 0.001 22.101 < 0.001 2007), these results suggest that the trophic ecology of these species is log(HL) × sex 3.246 0.0775 3.685 0.0605 more important than phylogenetic relatedness in shaping the mor- phology of these lizards. If antagonistic interactions between males consumption of harder items, including plants, in older individuals. were the only factor causing the observed changes in head morphology When comparing the head dimensions between sexes, males showed in M. thoracicus we would expect to find similar head morphologies in taller heads than females when we removed the effect of SVL (Fig. 2F) the other species as well. There is a high degree of antagonistic inter- and wider and taller heads when we removed the effect of HL (Fig. 3C action in this group as territoriality is common in Microlophus and D). Sexual dimorphism in head dimensions is commonly reported (Carpenter, 1966; Heisig, 1993; Watkins, 1996; Vidal et al., 2002) and

Table 4 ANCOVA results for comparisons of head traits between the groups including the three Microlophus species (M. thoracicus separated in juveniles and adults) with SVL (top) and HL as a covariate (bottom). Significant p–values are showed in bold.

log(HL) log(HW) log(HH)

F p F p F p

log(SVL) 1575.585 < 0.001 4558.42 < 0.001 2958.868 < 0.001 Groups 6.296 < 0.001 19.11 < 0.001 8.445 < 0.001 log(SVL) × species 9.907 < 0.001 4.32 0.006 7.29 < 0.001 log(HL) –– 2603.392 < 0.001 1323.33 < 0.001 Groups –– 60.954 < 0.001 36.817 < 0.001 log(HL) × species –– 4.138 0.007 3.448 0.018

50 K.S. Toyama et al. Zoology 129 (2018) 45–53

Table 5 Morphological differences between species (M. thoracicus separated as juveniles and adults) when SVL or HL act as covariates. Above the diagonal p-values are shown if pairwise comparisons were possible. An interval representing the limits of a non-significance region is shown when different slopes made pair- wise comparisons not possible. Below the diagonal the name of the group with significantly largest values for a given trait is shown, “equal” is shown when no differences were found. JN is shown when Johnson–Neyman regions needed to be calculated. Groups are coded as “thor a” (adult M. thoracicus), “thor j” (ju- venile M. thoracicus), “per” (M. peruvianus) and “occi” (M. occipitalis).

thor a thor j per occi

HL ∼ SVL – p = 0.779 (4.09 – 4.36) p = 0.252 HW ∼ SVL – (4.06 – 4.38) p < 0.001 (3.65 – 3.90) thor a HH ∼ SVL – p = 0.03 p < 0.001 (3.68 – 3.91) HW ∼ HL – (2.87 – 3.17) p < 0.001 (3.21 – 3.41) HH ∼ HL – (2.79 – 3.02) p < 0.001 p < 0.001

HL ∼ SVL equal – (4.08 – 4.33) p = 0.101 HW ∼ SVL JN – p < 0.001 p < 0.001 thor j HH ∼ SVL thor j – p = 0.005 (3.49 – 3.78) HW ∼ HL JN – p = 0.090 p < 0.001 HH ∼ HL JN – (2.67 – 2.98) p = 0.04

HL ∼ SVL JN JN – (4.23 – 4.41) HW ∼ SVL thor a thor j – (3.74 – 4.15) per HH ∼ SVL thor a thor j – (3.65 – 4.09) HW ∼ HL thor a equal – (3.23 – 3.50) HH ∼ HL thor a JN – p < 0.001

HL ∼ SVL equal equal JN – HW ∼ SVL thor a thor j JN – occi HH ∼ SVL JN JN JN – HW ∼ HL JN thor j JN – HH ∼ HL thor a thor j per – has been also observed in M. thoracicus (pers. observations). In contrast, if diet was responsible for the observed differences, we would get the pattern we observed here, that M. thoracicus has a more robust skull than its equally territorial congeners. Similar results were obtained when removing the effect of HL. Interestingly, in this case adults of M. thoracicus always showed the highest and widest heads when compared to the other groups (Fig. 5), while juvenile M. thoracicus showed head shapes more similar to that of M. peruvianus and M. occipitalis, which is Fig. 4. Ontogeny of head dimensions in Microlophus species. Allometric re- in accordance with their more similar dietary habits. These results lationships of (A) HL, (B) HW, and (C) HH with SVL for the four Microlophus groups (M. occipitalis: n = 77; R2 for HL = 0.770, HW = 0.823, HH = 0.707; suggest that there is a link between diet characteristics and head all p < 0.001. M. peruvianus: n = 49; R2 for HL = 0.869, HW = 0.913, morphology that extends and changes across life stages in these lizards, HH = 0.874; all p < 0.001. Values for M. thoracicus are shown in Fig. 2). following ecomorphological patterns found in previous studies (Herrel Comparisons were done based on the logarithm transformation of head traits et al., 2001a, 2001b; 2006; 2008; Kohlsdorf et al., 2008; Dollion et al., and SVL. Legend shown in figure. 2017) and supporting previous work that demonstrated the variability of head shape in tropidurids in respect to ecological factors (Kohlsdorf plant-rich diet and found that the dimensions of individuals ’ small in- et al., 2008; Toyama, 2017). However, the differences in head mor- testines and hindguts increased, and that their microbial gut commu- phology between sexes indicate that head morphology might be shaped nities were enriched relative to control individuals. Together, the re- by sexual selection as well as natural selection in this species. Although sults of these studies suggest that morphological, physiological, and this interaction between selective pressures has been found to influence microbial constraints can be alleviated by phenotypic flexibility. The head morphology in other lizard species (e.g. Massetti et al., 2017; ontogenetic change in diet and ecomorphology described in this study Gomes et al., 2018), the extent to which each of them shape the mor- could be an example of phenotypic flexibility favoring the consumption phology of M. thoracicus requires further study. of different resources in different life stages instead of being a fixed Herbivory is a rare feeding strategy in reptiles. In fact, less than 4% evolutionary feature. To determine which is the case for M. thoracicus of squamate reptiles are herbivores and the strategy is restricted to li- future experimental studies using controlled diets could be performed zards (Espinoza et al., 2004; Kohl et al., 2016; Pietczak and Vieira, to posteriorly explore potential changes in the external and internal 2017). Some hypotheses attempted to explain the scarcity of herbivory morphology related to digestion. among lizards by suggesting that this feeding strategy is limited by physiological and microbial restrictions that prevent adequate digestion of plant material (Sokol, 1967; Pough, 1973; Ruppert, 1980; Karasov 5. Conclusions et al., 1986; Cooper and Vitt, 2002). However, recent studies have shown that lizards are able to rapidly evolve adaptations to overcome Our results confirmed the existence of a gradual ontogenetic change these constraints. Herrel et al. (2008) found that an increase in plant in the diet of the lizard M. thoracicus. As they age, individuals switch material consumption caused dramatic changes in head morphology from a diverse diet towards a mainly herbivorous one. Moreover, the and digestive tract structure on a short time scale. More recently, Kohl same progressive change in diet was observed in morphological traits et al. (2016) experimentally fed Liolaemus ruibali individuals with a that are known to be related to bite force, a measure of performance

51 K.S. Toyama et al. Zoology 129 (2018) 45–53

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