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. 2021 Mar 2;239(1):167–183. doi: 10.1111/joa.13416

Endocranial morphology of the piciformes (Aves, Coraciimorphae): Functional and ecological implications

María Manuela Demmel Ferreira 1,✉, Federico Javier Degrange 1, Germán Alfredo Tirao 2, Claudia Patricia Tambussi 1
PMCID: PMC8197964  PMID: 33655532

ABSTRACT

We used three‐dimensional digital models to investigate the brain and endosseous labyrinth morphology of selected Neotropical Piciformes (Picidae, Ramphastidae, Galbulidae and Bucconidae). Remarkably, the brain morphology of Galbulidae clearly separates from species of other families. The eminentiae sagittales of Galbulidae and Bucconidae (insectivorous with high aerial maneuverability abilities) are smaller than those of the toucans (scansorial frugivores). Galbula showed the proportionally largest cerebellum, and Ramphastidae showed the least foliated one. Optic lobes ratio relative to the telencephalic hemispheres showed a strong phylogenetic signal. Three hypotheses were tested: (a) insectivorous taxa that need precise and fast movements to catch their prey, have well developed eminentiae sagittales compared to fruit eaters, (b) species that require high beak control would show larger cerebellum compared to other brain regions and higher number of visible folia and (c) there are marked differences between the brain shape of the four families studied here that bring valuable information of this interesting bird group. Hypotheses H1 and H2 are rejected, meanwhile H3 is accepted.

Keywords: brain vasculature, comparative neuroanatomy, endocasts, endosseous labyrinth, feeding behavior, neotropical piciformes

We use 3D digital models of the brain cavity and inner ear of species of Picidae, Ramphastidae, Galbulidae and Bucconidae to better understand functional and ecological implications. We found marked differences among the brains of the four families, being G. ruficauda the most different one. Fruit eaters (Ramphastidae) had the biggest eminenta sagittales ratio. The cerebellum showed variable sizes and variable visible foliation among species. Only the optic lobe ratio has a phylogenetic signal.

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1. INTRODUCTION

Piciformes (woodpeckers and allies) include nine families of arboreal birds. They are all zygodactyl, and have similarities in a tendon structure which is crucial for perching. Four families of the Order (Capitonidae, Megalaimidae, Lybiidae and Indicatoridae) are only found outside of the Americas. The remaining five families (Galbulidae, Bucconidae, Ramphastidae, Picidae and Semnornithidae) have representatives in the Neotropics but only four families (Galbulidae, Bucconidae, Ramphastidae and Semnornithidae) are exclusive of this region.

Galbulidae (Jacamars) and Bucconidae (Puffbirds) are sister families (Hackett et al., 2008; Livezey & Zusi, 2007; Prum et al., 2015). Both families are comprised by small to medium‐sized birds that use the beak to catch insects during flight. Picidae (woodpeckers) are a well‐defined clade (Winkler et al., 2014 and literature cited therein) with a worldwide distribution, except for the Australo‐Papuan region (Benz et al., 2006). They are insectivorous, adapted to climbing, with a specialized foraging strategy and a unique capacity to extract insects from woody substrates (Benz et al., 2006; Manegold & Töpfer, 2012). Ramphastidae (toucans) are native to the Neotropics, mostly forest and jungle inhabitants. They feed mostly on fruits, but also on flowers, arthropods and small vertebrates (Galetti et al., 2000). Semnornithidae (toucan barbets) are inhabitants of humid montane forests that live in small family groups. Adults feed on fruits and a variety of animal prey, but the chicks are insectivorous. They are considered to be phylogenetically close to toucans.

Endocranial morphology varies across Aves; nevertheless, variation among related species remains mainly unknown (Smith & Clarke, 2012). Starting from this base, we used three‐dimensional models to explore brain morphology of selected Neotropical Piciformes (i.e., puffbirds, jacamars, toucans, woodpeckers and allies). Our main objective was to investigate the brain, vasculature and endosseous labyrinth morphology, in order to identify possible differences and similarities within the neotropical members of this avian group.

In birds, the external anatomy of the brain has proven to be a rich source of information applicable in systematics, evolution and ecology (Iwaniuk & Hurd, 2005; Smith & Clarke, 2012). It is consensually assumed that the capacities an individual can display or the speed response to certain stimulus are related to the size of a specific brain structure. This concept is known as Principle of Proper Mass of Jerison (1973), and states that “the size of a neural structure that is associated with certain behaviors is a reflection of the complexity of such behaviors” (Wylie et al., 2015: 2).

It is known that the size of the eminentiae sagittales, or Wulsts, is related to visual and somatosensory inputs and can be used as a proxy of these capacities (Boire et al., 2002; Early et al., 2020b, 2020a,2020b, 2020a; Iwaniuk et al., 2007a; Iwaniuk & Wylie, 2007; Ksepka et al., 2012; Medina & Reiner, 2000; Smith & Clarke, 2012; Timmermans et al., 2000; Wild & Williams, 1999; Wylie et al., 2015). This is why the underlying soft‐tissue structure, the hyperpallium, is part of the thalamofugal visual pathway. Furthermore, there is evidence that some of the neurons of the nuclei of the thalamofugal pathway have shown to be important for the coordination of motor output to the flight muscles (Brauth & Karten, 1977; Brecha et al. 1980; Clarke, 1977; Lau et al. 1998). Martin (2017) suggested that vision is mainly driven by foraging: the task of detecting and obtaining food is likely to pose a constant perceptual challenge in the majority, if not all, bird species. The mission of controlling the bill's location and position in foraging needs to be strongly precise and accurate. When the pray is evasive and mobile, the precision of bill position and the timing of its arrival at the food object are vital, since there is often only a single opportunity to take a particular item, or else it escapes (Martin, 2017). Pecking, snatching or lunging feeding techniques need a precise calculation of the position of an object as it is approached and an accurate estimate of time to contact that item in order to coordinate the opening of the bill is also crucial (Martin, 2009). So, first we hypothesized (H1) that insectivorous taxa that catch their prey during flight that need precise and fast movements to catch their prey, have well developed eminentiae sagittales compared to fruit eaters.

The cerebellum can be subdivided into individual folia, which receive different combinations of somatosensory input from different parts of the body. Enlargement of the number of cerebellar foliations has been associated with major density of cerebellar neural circuitry, which allows an improvement of the processing capacity and motor abilities, specifically manipulative skills (Butler & Hoods, 2005; Hall et al., 2013; Iwaniuk et al., 2009; Wylie et al., 2018). There is a positive correlation between cerebellar foliation and tool use in birds (Iwaniuk et al., 2009) and between the enlargement of the cerebellum and beak control (Sultan & Glickstein, 2007). We hypothesize (H2) that Piciformes species that require a very precise movement of the head and beak will have larger cerebella with greater number of folds.

Brain shape has been proven to be related with behavior, ecological or even phylogenetic aspects (Iwaniuk & Hurd, 2005). Assuming that the different skills and habits exhibited by the Piciformes are reflected in the shape of the brain, we thirdly hypothesize (H3) that we will find marked and substantial differences in the brain of the species studied here.

Our main objective was to investigate the brain, vasculature, and endosseous labyrinth morphology, and to assess whether the possible morphological similarity within the Neotropical members of Coraciimorphae are or are not related to functional convergences. With this study we aim to contribute to the database of brain anatomy of living Neotropical Piciformes. We are convinced that our results will benefit future phylogenetic and / or functional investigations of these birds.

2. MATERIALS AND METHODS

The use of computed tomographies for 3D modeling is a non‐destructive technique that is widely used to visualize and identify different anatomical structures (Balanoff et al., 2015; Early et al., 2020b, 2020a,2020b, 2020a; Watanabe et al., 2018). Since the meninges are so thin, the avian brain fills almost the whole endocranial cavity and copies its shape perfectly. The resulting brain endocast can be considered as an excellent proxy for brain morphology and volume (Balanoff et al., 2015; Iwakiuk & Nelson, 2002; Striedter, 2005; Walsh & Milner, 2011; Watanabe et al., 2018). This tool facilitates comparisons, since the datasets obtained are easy to manipulate and share (Carril et al., 2015).

We sampled collected museum specimens currently recognized for Neotropical Piciformes families (Picidae, Galbulidae, Bucconidae, Ramphastidae; endocasts of Semnornithidae were not available). No live animals were collected for this study. Eleven skulls (Figure 1) of adult Piciformes (Picidae: Colaptes campestris (Vieillot, 1818) CIT‐O811, Colaptes melanochloros (Gmelin, 1788) MZUC (one female and one male), CIT‐O19 (freezer collection); Colaptes pitius (Molina, 1782), CIT‐O103 and Melanerpes cactorum (D'Orbigny, 1840) MZUC; Ramphastidae: Ramphastos toco (Statius Muller, 1785) MZUC, and Ramphastos vitellinus (Lichtenstein, 1823) CIT‐O314; Galbulidae: Galbula ruficauda (Cuvier, 1816) CIT‐O319), and Bucconidae: Nystalus maculatus (Gmelin, 1788) CIT‐O72 and Monasa nigrifrons (Spix, 1824) CIT‐O330) were scanned. Specimens are housed at the Colección Osteológica de Aves of the Centro de Investigaciones en Ciencias de la Tierra (“CICTERRA”) (CIT‐O) and the Museo de Zoología de la Universidad Nacional de Córdoba (“MZUC”), Argentina.

FIGURE 1.

FIGURE 1

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Phylogeny of subset 11 species of Coraciimorphae clade, where the endocasts are shown inside the skull. The Trogon viridis and Chloroceryle amazona are included as outgroups. The heads are in the ‘alert’ postures, with skull oriented so that the horizontal semi‐circular canal is parallel to the ground. The simplified tree was taken from Prum et al. (2015). Scale = 1 cm

The skulls were scanned with a non‐commercial equipment developed by researchers of Grupo de Espectroscopía Atómica y Nuclear (“GEAN”) at the Facultad de Matemática, Astronomía y Física (“FaMAF”), Córdoba province, Argentina. With this equipment it is possible to obtain 2D images up to 20 cm × 20 cm with a pixel size of 194 μm2. The equipment uses a conventional X‐ray source with an anode of W. The images were taken using an accelerating voltage of 30 kV and filters of Zr and Al to modulate the beam energy distribution. The mathematical reconstruction was made with 1,600 projections, equally distributed in 360º, using the filtered backprojection (FBP) algorithm. This algorithm, based on the Radon inverse transformation, is a very efficient and therefore a widely used reconstruction method (Hsieh, 2009). The FBP algorithm was implemented with a Shepp‐Logan filter and spline interpolation.

DICOM files were processed and resampled (voxel size: 0.1 mm) using Avizo (Version 7.1). Anatomical structures such as endocast, inner ear, nerves and blood vessels were manually segmented and three‐dimensional (3D) models were generated.

Measurements of brain endocasts were taken from the 3D models (see Table 1) following Tambussi et al. (2015), adding other measurements (e.g., length and wide of the medulla). These measurements attempt to supply quantitative information about shape and size of the different brain structures. The measurements were taken as linear distances in millimeters, using Avizo tools by the first author in order to avoid interobserver error. With those measurements, indexes were calculated (see Table 2). Body mass was taken from Dunning (2008) and brain volumes were calculated with Avizo.

TABLE 1.

Measurements, brain volume and body mass of the specimens in this study

Family Bucconidae Galbulidae Picidae Ramphastidae
Species Nystalus maculatus Monasa nigrifrons Galbula ruficauda Colaptes melanochloros a Colaptes pitius Colaptes campestris Melanerpes cactorum Ramphastos toco Ramphastos vitellinus
Brain Volume 962.1 1524.76 492.46 3362.77 4069 3703.06 1548.15 6468.9 5728.52
Body Mass 42 80.7 26.5 127.75 159 158 35.05 618 343.5
Bulbus Olfactorius 0.69 0.62 0.52 2.40 2.51 2.34 1.09 2.63 3.05
Cerebellum Length 8.11 8.39 7.38 8.63 9.77 7.66 7.35 14.26 12.84
Cerebellum Width 4.81 4.93 3.91 7.97 8.9 7.52 5.97 10.3 8.54
Floccular Length 0.74 0.65 0.9 2.46 2.36 2.29 1.76 2.72 1.84
Telencephalic Hemisphere Length 8.69 11.27 7.19 20.09 20.98 20.44 14.11 19.14 21.37
Telencephalic Width 16.56 19.8 12.74 21.90 23.85 23.73 18.01 31 29.51
Optic Lobe max. Height 4.49 5.45 5.29 3.62 4.95 5.56 3.61 6.3 6.78
Optic Lobe max. Length 6.37 8.48 2.79 7.58 7.9 7.74 5.35 10.74 10.53
Wulst max. Length 6.32 9.91 3.26 16.75 17.72 18.01 12.51 17.98 16.95
Wulst max. Width 2.43 3.81 1.92 7.40 7.65 7.95 5.69 6.14 5.87
Medulla Oblongata Length 4.93 6.35 4.67 7.98 6.81 6.72 4.41 8.77 7.64
Medulla Oblongata Width 2.45 3.33 2.37 4.13 2.81 3.16 2.3 4.78 4.57
1 59.3 52.7 42.3 13.9 15.9 16.5 18 20.04 13.8
2 45.2 52.6 41.1 36.1 32.6 29.7 41.4 40 31.8
3 13.6 4.8 7.1 20.09 17.9 15.9 26.3 24.7 21.3
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Abbreviations: 1, angle between brain plane (brp) and plane of lamina parasphenoidalis (plp); 2, angle between brp and horizontal semi‐circular canal (hsp); 3, angle between hsp and plp. Measurements in mm; Body Mass in g; Brain Volume in mm3. Angles in degrees. See Tambussi et al. (2015) for more information.

a

Values correspond to average measurements from 3 specimens: Colaptes melanochloros MZUC (one female and one male) and CIT‐O19 (freezer collection).

TABLE 2.

Indices recovered from measurements in Table 1

Family Bucconidae Galbulidae Picidae Ramphastidae
Species Nystalus maculatus Monasa nigrifrons Galbula ruficauda Colaptes melanochloros a Colaptes pitius Colaptes campestris Melanerpes cactorum Ramphastos toco Ramphastos vitellinus
Telencephalic Width/Telencephalic Hemisphere Length 1.90 1.76 1.77 1.09 1.14 1.16 1.28 1.62 1.38
OR % 7.94 5.50 7.23 11.95 11.96 11.45 7.72 13.74 14.27
Cerebellum Width/Cerebellum Length 0.59 0.59 0.53 0.92 0.91 0.98 0.81 0.72 0.66
Wulst Length /Telencephalic Hemisphere Length 0.73 0.88 0.45 0.83 0.84 0.88 0.89 0.94 0.79
OLR % 73.30 75.24 38.80 37.67 37.65 37.87 37.92 56.11 49.27
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OLR, optic lobe ratio = (Optic Lobe Height/Telencephalic Hemisphere Length) × 100; OR, olfactory ratio = (Bulbus Olfactorius/Telencephalic Hemisphere Length) × 100.

a

Values correspond to average measurements from 3 specimens: Colaptes melanochloros MZUC (one female and one male) and CIT‐O19 (freezer collection).

Brain anatomical terminology for the central nervous system primarily follows Breazile and Kuenzel (1993), with English equivalents of Latin terms.

It was performed regression (OLS model) between brain volume and body mass. Using the Prum et al. (2015) phylogenetic proposal, phylogenetic correction for the regression analysis was performed using the pgls function (Phylogenetic Generalized Linear Models) of the phytools package (Revell, 2012) in RStudio 3.4.3. Endocranial volumes were taken from Walsh et al. (2013), Carril et al. (2015), Tambussi et al. (2015) and the volumes obtained in the present work.

The amount of phylogenetic signal was assessed for the indexes calculated from the measurements mentioned above (see Table 2) based on the phylogenetic proposal of Prum et al. (2015). For this, the kappa statistic (K) of Bloomber et al. (2003) was calculated under a Brownian motion model of evolution. The test was performed using the phylosignal function from the Picante package (Kembel et al., 2010) in Rstudio 3.4.3.

The hearing range (Hz) and mean hearing (Hz) were calculated following Walsh et al. (2009) (Table 3).

TABLE 3.

Mean hearing (Hz) and hearing range (Hz) estimations recovered in this study

Family Bucconidae Galbulidae Picidae Ramphastidae
Species Nystalus maculatus Monasa nigrifrons Galbula ruficauda Colaptes melanochloros a Colaptes pitius Colaptes campestris Melanerpes cactorum Ramphastos toco Ramphastos vitellinus
Cochlear Duct Length 3.91 4.42 2.424 4.57 4.4 5.21 2.9 6.505 5.48
Basicranial Length 7.09 7.33 3.9 10.27 12.83 11.28 7.88 13.02 10.43
Cochlear Duct Length/Basicranial Length 0.55 0.60 0.62 0.44 0.34 0.46 0.36 0.50 0.52
log10 Cochlear Duct Length /Basicranial Length −0.26 −0.22 −0.21 −0.35 −0.47 −0.34 −0.43 −0.30 −0.28
Best Hearing Range 5397.42 5634.2 5714.47 4822.80 4138.08 4927.38 4325.15 5135.59 5269.03
Mean Hearing Range 3144.93 3273.37 3316.91 2833.22 2461.79 2889.95 2563.27 3002.89 3075.28
Lower Limit Hearing Range 446.22 456.27 459.68 421.82 392.75 426.26 400.69 435.10 440.77
Upper Limit Hearing Range 5843.64 6090.47 6174.14 5244.62 4530.83 5353.64 4725.85 5570.69 5709.79
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a

Values correspond to average measurements from 3 specimens: Colaptes melanochloros MZUC (one female and one male) and CIT‐O19 (freezer collection).

3. RESULTS

3.1. Description of the brain

Regression analysis (Figure 2) shows that Bucconidae, Picidae and Ramphastidae have larger brains than expected for a bird of their body mass. And Galbula ruficauda is the only one which has a lower brain volume than expected for a bird of its body mass.

FIGURE 2.

FIGURE 2

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Regression analyses between endocranial volume and body mass of Piciformes. Interrupted line represents the corrected phylogenetically regression line (pgls; y = 0.585x + 1.9275, r 2 = 0.802, p = 0.000); whereas continuous line represents the regression without phylogenetic correction (OLS model; y = 0.5019x + 2.3081, r 2 = 0.7612, p = 0.000). 1, Galbula ruficauda (Galbulidae); 2, Nystalus maculatus (Bucconidae); 3, Monasa nigrifrons (Bucconidae); 4, Melanerpes cactorum (Picidae); 5, Colaptes melanochloros (Picidae); 6, Colaptes pitius (Picidae); 7, Colaptes campestris (Picidae); 8, Ramphastos toco (Ramphastidae); 9, Ramphastos vitellinus (Ramphastidae); 10, Ramphastos dicolorus (Ramphastidae)

All the endocasts reconstructed in this study belong to an airencephalic type of brain (Hofer, 1952) (Figure 3), characterized by a dorsal position of the brain with respect to the rostrum, with a substantial dorsoventral superposition of the hemispheres, optic lobes and medulla oblongata, although there are minimal differences in the degree of superposition of the telencephalon on the cerebellum among the studied species.

FIGURE 3.

FIGURE 3

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Cranial endocasts reconstructed from CT scans. From left to right: dorsal, ventral, lateral, rostral and caudal views. a, Galbula ruficauda CIT‐O319 (Galbulidae); b, Monasa nigrifrons CIT‐O142 (Bucconidae); c, Nystalus maculatus CIT‐O72 (Bucconidae); d, Colaptes melanochloros MZUC (Picidae); e, Colaptes campestris CIT‐O811(Picidae); f, Colaptes pitius CIT‐O103 (Picidae); g, Melanerpes cactorum MZUC (Picidae); h, Ramphastos toco MZUC (Ramphastidae); i, Ramphastos vitellinus CIT‐O330 (Ramphastidae). Scale in a = 0.25 cm. Scale from b–i = 0.5 cm

3.1.1. Telencephalon

The telencephalon in Galbulidae is wider than long (Figure 4a) as a consequence of having telencephalic hemispheres laterally expanded (Tables 1, 2). The fissura interhemispherica is poorly marked in Galbulidae but narrow and shallow in Bucconidae. In Bucconidae, the eminentiae sagittales are long, more expanded rostrocaudally, meanwhile in Galbula the eminentiae are more rostrally placed. However, in both families they are low in height, poorly dorsally extended. Seen dorsally in Monasa nigrifrons (Black‐fronted Nunbird), the eminentiae sagittales gradually expand towards the caudal portion. The vallecula is almost imperceptible in both Galbula ruficauda and Nystalus maculatus, but it is well‐marked in M. nigrifrons. Olfactory bulbs are unnoticeable in Galbulidae (Figure 5a). The olfactory ratio among Bucconidae (from 7.94% to 5.50%, Table 2) is small.

FIGURE 4.

FIGURE 4

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Cranial endocasts reconstructed from CT scans in dorsal view. a, Galbula ruficauda CIT‐O319 (Galbulidae); b, Monasa nigrifrons CIT‐O142 (Bucconidae); c, Colaptes melanochloros MZUC (Picidae); d, Ramphastos toco MZUC (Ramphastidae). Abbreviations: ce, cerebellum; cf, cerebellar folds; fi, fissura interhemispherica; hsc, horizontal semi‐circular canal; psc, posterior semi‐circular canal; so, sinus occipitalis; th, telencephalic hemisphere; v, valeculla; voe, vena occipitalis externa; w, wulst. I‐XII, cranial nerves. Scale in a = 0.25 cm. Scale from b–d = 0.5 cm

FIGURE 5.

FIGURE 5

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Cranial endocasts reconstructed from CT scans in ventral view. a, Galbula ruficauda CIT‐O319 (Galbulidae); b, Monasa nigrifrons CIT‐O142 (Bucconidae); c, Colaptes melanochloros MZUC (Picidae); d, Ramphastos toco MZUC (Ramphastidae). Abbreviations: ce, cerebellum; ca, carotids; fm, fissura mediana, hsc, horizontal semi‐circular canal; ob, olfactory bulb; ol, optic lobe; p, pituitary gland (hypophysis); psc, posterior semi‐circular canal; th, telencephalic hemisphere; voe, vena occipitalis externa; I‐XII, cranial nerves. Scale in a = 0.25 cm. Scale from b–d = 0.5 cm

The telencephalon of Picidae is almost as wide as long (Tables 1, 2), sub‐rounded when viewed dorsally. The eminentiae sagittales are caudally wider, very long, conspicuous (Figure 4c‐d, Table 1), and they end at the caudal limit of the telencephalic hemisphere (Figure 6c). In Colaptes campestris, the eminentiae sagittales have a slight constriction at the rostral end. Both the fissura interhemispherica and the vallecula of the Picidae studied are very well marked, narrow and shallow (Figure 4c). The olfactory bulbs are small but conspicuous, with well‐marked limits. The olfactory ratios are also small (Table 2).

FIGURE 6.

FIGURE 6

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Cranial endocasts reconstructed from CT scans in caudal view. a, Galbula ruficauda CIT‐O319 (Galbulidae); b, Monasa nigrifrons CIT‐O142 (Bucconidae); c, Colaptes melanochloros MZUC (Picidae); d, Ramphastos toco MZUC (Ramphastidae). Abbreviations: asc, anterior semi‐circular canal; ca, carotids; cf, cerebellar folds; fic, fissure cerebelli; fl, floculli; hsc, horizontal semi‐circular canal; mo, medulla oblongata; ob, olfactory bulb; ol, optic lobe; p, pituitary gland (hypophysis); psc, posterior semi‐circular canal; so, sinus occipitalis; th, telencephalic hemisphere; voe, vena occipitalis externa; w, wulst. I‐XII, cranial nerves. Scale in a = 0.25 cm. Scale from b–d = 0.5 cm

In Ramphastidae, the telencephalic hemispheres are rather wider than longer (Tables 1, 2). The eminentiae sagittales are conspicuous, narrow and very elongated rostrocaudally in dorsal view (Figure 3c‐d, Table 1), ending they at the caudal limit of the telencephalic hemispheres, too. (Figure 6d). They are more rostrally extended than in Picidae. The fissura interhemispherica is deep, wide and pronounced (Figure 4d). The vallecula is inconspicuous. Olfactory bulbs are located directly at the rostral end of the telencephalon. They are small (the olfactory ratios are about 15% of the telencephalon length, Table 1), however noticeable. Both Ramphastidae specimens have two conspicuous lumps ventrocaudally to the bulbus olfactorius (Figures 5d, 7d). Due to the position, these might belong to the mesopallium or the nidopallium, both regions involved in learning and memory process (Nomura & Izawa, 2017).

FIGURE 7.

FIGURE 7

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Cranial endocasts reconstructed from CT scans in rostral view. a, Galbula ruficauda CIT‐O319 (Galbulidae); b, Monasa nigrifrons CIT‐O142 (Bucconidae); c, Colaptes melanochloros MZUC (Picidae); d, Ramphastos toco MZUC (Ramphastidae). Abbreviations: c, cochlea; ca, carotids; fi, fissura interhemispherica; hsc, horizontal semi‐circular canal; mo, medulla oblongata; ob, olfactory bulb; ol, optic lobe; p, pituitary gland (hypophysis); psc, posterior semi‐circular canal; so, sinus occipitalis; th, telencephalic hemisphere; voe, vena occipitalis externa; w, wulst. I‐XII, cranial nerves. Scale in a = 0.25 cm. Scale from b–d = 0.5 cm

3.1.2. Diencephalon

The pineal gland could not be reconstructed as it did not leave an impression on the available endocasts. The hypophysis in Galbula ruficauda is small and blunt (Figure 7a). In Galbula and Nystalus is slightly projected rostrally when viewed laterally. In the remaining specimens analyzed here, it is very stout, dorsoventrally expanded and ventrally rounded. In Picidae, the gland displays, on its ventral portion, a small protrusion rostrally directed (Figure 7c). In Monasa, Picidae and Ramphastidae it is oriented perpendicularly to the horizontal semi‐circular canal of the inner ear (see below).

3.1.3. Mesencephalon

Virtual endocasts of G. ruficauda and Bucconidae exhibit large optic lobes. These are more caudodorsally oriented in G. ruficauda than in Bucconidae when viewed laterally (Figure 8a,b). In particular, they are more robust and kidney‐shaped in Monasa than in Nystalus. In both specimens, the length of the optic lobe is circa 74% of the total telencephalic hemisphere length, whereas in Galbulidae they represent near 39% of the total telencephalic hemisphere length (Table 2). In both families, the telencephalic hemispheres completely overlap the tectum opticum and as a consequence they cannot be observed in dorsal view (Figure 4a‐b). In fact, this is a frequent feature in most birds (Milner & Walsh, 2009; Smith & Clarke, 2012), and therefore it is not surprising that this is also the case in Picidae and Ramphastidae (Figure 4c‐d). Moreover the optic lobes of Picidae are partially overlapped by ventrolateral projections of the telencephalic hemispheres (Figure 8c), a feature absent in Ramphastidae that seems to be exclusive of this family.

FIGURE 8.

FIGURE 8

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Cranial endocasts reconstructed from CT scans in left lateral view. a, Galbula ruficauda CIT‐O319 (Galbulidae); b, Monasa nigrifrons CIT‐O142 (Bucconidae); c, Colaptes melanochloros MZUC (Picidae); d, Ramphastos toco MZUC (Ramphastidae). Abbreviations: asc, anterior semi‐circular canal; ca, carotids; cf, cerebellar folds; fic, fissure cerebelli; fl, floculli; hsc, horizontal semi‐circular canal; mo, medulla oblongata; ob, olfactory bulb; ol, optic lobe; p, pituitary gland (hypophysis); psc, posterior semi‐circular canal; so, sinus occipitalis; th, telencephalic hemisphere; voe, vena occipitalis externa; w, wulst. I‐XII, cranial nerves. Scale in a = 0.25 cm. Scale from b–d = 0.5 cm

In Bucconidae, the tectum opticum is displaced more rostrally, while in Galbulidae it is more caudally, towards the cerebellum (Figure 8a‐b). There is a deep groove between the telencephalic hemispheres and the tectum opticum extending caudally to contact with the cerebellum in M. nigrifrons and G. ruficauda.

The optic lobes are suboval in Melanerpes cactorum and kidney‐shaped in Colaptes as in Ramphastidae. Ramphastos have large optic lobes, rostrally displaced. They are as long as half the length of the telencephalic hemispheres (Table 2).

3.1.4. Metencephalon

In both Galbulidae and Bucconidae, the cerebellum is longer than wider. Due to the proportionally smaller size of the telencephalon, the cerebellum of Galbulidae seems to be more protruded caudally than in Bucconidae in lateral and dorsal views (Figures 4a, 8a). Specimens of Galbulidae show seven cerebellar folds, whereas specimens of Bucconidae have five in Monasa and four in Nystalus (Figures 4a,b, 8a,b). The contact of the cerebellum with the telencephalon is slightly “V” shaped in Galbula (Figure 6a). It is straight in Bucconidae (Figure 6b). The flocculi of the Bucconidae are small and conical, scarcely projecting laterally (Figure 7b) and barely visible in dorsal view. In Galbula, they are more robust, slenderly laterally projected, observable when viewed dorsally.

In Picidae, the cerebellum is as long as wide with four to six folia. The limit between the telencephalon and the cerebellum has a clear “V” shape (Figure 6c). Flocculi are not visible dorsally due to their small size and poor lateral projection. In all Picidae, the flocculi have a sub‐conical shape and they are projected caudoventrally, except for Melanerpes cactorum, where the flocculi are shorter than the rest of the members of the family. In Ramphastidae, the cerebellum is elongated and its contact with the telencephalon is straight (Figure 6d). There are four visible folds. The flocculi are stout, caudoventrally curved, not observable in dorsal view.

3.1.5. Myelencephalon

In Bucconidae, the medulla oblongata is sub‐rounded (Figure 5b), lies in a plane perpendicular to the telencephalic hemispheres, and ventrorostrally to the cerebellum. The fissura mediana is short and shallow. In G. ruficauda, the medulla oblongata (Figures 5a, 7a), is also sub‐rounded, located more caudally when viewed laterally and not located in a perpendicular plane with respect to the telencephalic hemispheres. The fissura mediana is deep and well defined.

Picidae and Ramphastidae have a more sub‐horizontally disposition of the medulla regarding the lateral semi‐circular canal. In Picidae, the medulla oblongata is globose (Figures 5c, 7c) and placed rostrally regarding the cerebellum. The fissura mediana is wide and deep. Ramphastidae have a medulla oblongata more caudally disposed. The fissura mediana is shallow, less noticeable than in Picidae (Figures 5d, 7d).

3.2. Cranial nerves

The olfactory nerve (cranial nerve I) is represented by a small lump at the cranial end of the bulbus olfactory. This nerve is short and small in G. ruficauda and Bucconidae when compared with the other families. In Picidae, cranial nerve I is long and thin, while in Ramphastidae is short but stouter than in Picidae.

Optic nerve (cranial nerve II) is placed at the exit of the diencephalon. Based on the relationship between the optic foramina and the optic nerve, Hall et al. (2009) distinguish four types of optic foramina: type 1 when there is a single optic foramen present in each orbit that probably reflects the size of the optic nerve; type 2 when there is a single central optic foramen that probably belongs to the optic chiasm; type 3 when the foramina are large and do not reflect the size of the optic nerve, and type 4, there is no optic foramen since the posterior wall of the orbit is not ossified. Monasa nigrifrons fits into type 1, while Galbula, Nystalus, Ramphastidae and Picidae into type 3.

The oculomotor nerve (cranial nerve III), which is generally located dorsolaterally to cranial nerve IV, was only identified in Picidae. (Figure 7c). The trochlear cranial nerve IV is small and points caudally in Galbula; it is bigger, stouter and directed cranially in Bucconidae whereas it is robust and cranially orientated in Picidae and Ramphastidae.

It was only possible to reconstruct completely the trigeminal nerve (cranial nerve V) in Picidae where it was possible to identify the main branches of this nerve (Figure 5c,). It was not possible to reconstruct this nerve completely in G. ruficauda, Bucconidae and Ramphastidae. Abducens nerve (Cranial nerve VI) was only identified and reconstructed in Picidae (Figure 5c). It is a small bump directed rostrally.

Facial and vestibulocochlear nerves (cranial nerves VII and VIII) look like a small bump in Galbula ruficauda. In Bucconidae, it was not possible to identify them (Figure 8a). In Picidae both nerves are wider, partially covered by the inner ear (Figure 8c). In Ramphastidae, these nerves have a small a narrow origin, located rostrally to the inner ear (Figure 8d).

As in most birds, glossopharyngeal, vagus and accessory cranial nerves IX to XI have a common origin. In G. ruficauda and Bucconidae they have a narrow origin but in Picidae the origin is large and wide. In Ramphastiade, the origin is narrower, even more than in Bucconidae and G. ruficauda.

The hypoglossal nerve (Cranial nerve XII) in Galbula and Ramphastidae is rounded in cross section, whereas in Picidae is flattened. It was not plausible to identify and reconstruct this nerve in Bucconidae.

3.3. Vasculature

In the neotropical Piciformes studied here, the left and right cerebral carotids may be connected by a highly visible transverse vessel that forms an H‐shaped intercarotid anastomosis or a side‐to‐side connection, resembling an X (Aslan et al., 2006; Baumel & Gerchman, 1968). Ramphastidae and Picidae have the first type while Galbulidae and Bucconidae have the second one. In all the specimens, two bony carotid canals traverse the base of the skull. In most birds, these canals provide passage for the arteria carotis cerebralis and, generally, also conduct the vena carotis cerebralis.

In Galbulidae and Bucconidae the vena occipitalis externa is thin and curved following the anterior semi‐circular canal. In Picidae it becomes thicker in the most dorsal portion, but in Ramphastidae it has the same section throughout all its path. In these last two families, their trajectory follows the shape of the metencephalon.

The sinus occipitalis is small, running through the mid‐line dorsal surface of the cerebellum in G. ruficauda. The sinus occipitalis is sharp, well‐marked and bifurcates ventrocaudally in M. nigrifrons. It was not possible to identify the sinus in N. maculatus. In Picidae and Ramphastidae, the cerebellar folds are visible (especially in Melanerpes), indicating that the sinus occipitalis is poorly developed.

3.4. Endosseous Labyrinth

In Galbulidae and Bucconidae, the three semi‐circular canals are sub‐circular in cross section with the anterior semi‐circular canal (ASC) being more expanded. This condition is less evident in G. ruficauda, which has the three semi‐circular canals more robust and less extended. All ampullae are stout and prominent in N. maculatus. In M. nigrifrons only the anterior ampulla has a greater development than the others. The ampullae on G. ruficauda are small and inconspicuous (Figure 9A). The crus commune is absent in N. maculatus; it is very small in G. ruficauda and it is almost imperceptible in M. nigrifrons. The ductus cochlearis in Bucconidae thins rostrally and is oriented obliquely with respect to the longitudinal axis of the skull. In G. ruficauda, the ductus cochlearis also thins rostrally, however, has a slight curvature toward the medial position.

FIGURE 9.

FIGURE 9

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Endocast of the left endosseous labyrinth. From left to right: lateral, cranial, caudal and dorsal views. a, Galbula ruficauda CIT‐O319 (Galbulidae); b, Monasa nigrifrons CIT‐O142 (Bucconidae); c, Colaptes melanochloros MZUC (Picidae); d, Ramphastos toco MZUC (Ramphastidae). Abbreviations: aa, anterior ampulla; asc, anterior semi‐circular canal; c, cochlea; cc, crus commune; fc, fenestra cochlearis; fv, fenestra vestibularis; la, lateral ampulla; hsc, horizontal semi‐circular canal; pa, caudal ampulla; psc, posterior semi‐circular canal. Scale: 0.25 mm

The semi‐circular canals in Picidae are subcircular in cross‐section, and both the anterior and the horizontal semi‐circular canals (HSC) are well developed. The connection between the ASC and the crus commune is perpendicular to the HSC (Figure 9c). The crus commune is short but distinguishable. The three ampullae look like detached from the main body of the inner ear, being the ampulla caudalis the stoutest. The ductus cochlearis is appreciably less robust in Colaptes cactorum than in the other Picidae. In the latter, the ductus is more developed, medially oriented, with a slight ventral curvature with respect to the position of the HSC. In Ramphastidae, the ASC is the most expanded, followed by the HSC. The crus commune is shorter than in Picidae but still distinguishable. The three ampullae are also detached and the most robust is the ampulla caudalis. The fenestra cochlearis is noticeably larger in Ramphastos vitellinus than in Ramphastos toco. The ductus cochlearis is robust and medially oriented in both specimens, however, in R. vitellinus it is also curved in the ventral direction.

4. DISCUSSION

We tested three hypotheses: first, we hypothesized that insectivorous taxa that catch their prey during flight that need precise and fast movements to catch their prey, have well developed eminentiae sagittales compared to fruit eaters. Second, species that require high and accurate beak control would show larger cerebellum compared to other brain regions and higher number of visible folia. Third, there are marked differences between the brain shapes of the four families studied here that could have systematic applications.

The results obtained in this work and the comparisons carried out allow us to test the three hypotheses raised and also present new information regarding other aspects of the brain, its vascularization and the inner ear.

Brain volume in birds has been associated with different features such as flight capacity (Bennett & Harvey, 1985; Corfield et al., 2008; Iwaniuk et al., 2004a), migratory behavior (Sol et al., 2010), developmental mode (Iwaniuk & Nelson, 2003), capacity to survive in nature (Sol et al., 2007), cognitive skills (Sol et al., 2004) and even social complexity (Burish et al., 2004). Also, differences in relative brain size can result from changes in body size, absolute brain size, or both (Jerison, 1973; Madden, 2001; Lefebvre et al., 1997, 2002; Cnotka et al., 2008; Overington et al., 2009).

As observed in Figure 2, all the specimens studied here have larger brains than expected for their body mass except for G. ruficauda. Ksepka et al. (2020) found that, in relation to other Telluraves, Coraciimorphae show a decrease in body size that leads them to show a higher slope in the co‐variation of the relationship with brain volume. Also, they found further decreases in body size within Picidae. Frugivorous Ramphastidae show higher brain volumes than the insectivorous Galbulidae and Bucconidae.

According to the calibrated phylogeny proposed by Prum et al. (2015) and the fossil record (Duhamel et al., 2020), Galbulidae and Bucconidae would have diverged from the rest of the Piciformes 50 to 54 million years ago, in the early Eocene. Sol and Price (2008) proposed that it is expected that early diverging families have had more opportunities, more habitat changes and more time for diversification than the younger ones. This is based on the existing link between ecology, behavioral plasticity and brain size (Lefebvre et al., 1997), indicating that having a larger brain might be a derived trait among Piciformes.

Nevertheless, changes in encephalization are not only related to selection on brain size alone (Ksepka et al., 2020). Recent studies propose that high levels of encephalization might be a result of differential growth of individual brain regions, such as those observed in owls, which have expanded Wulst (Balanoff et al., 2016; Iwaniuk et al., 2004b; Iwaniuk et al., 2005; Smaers & Vanier, 2019). Another explanation may be the increase in cognitive complexity, as observed in parrots and corvids (Ksepka et al., 2020). This might be a convergent increase in not only relative brain volume but also neuron density, allowing additional brain pathways or the elaboration or increased acuity of existing pathways (Ksepka et al., 2020).

Although all species showed an airencephalic type of brain (Hofer, 1952), the general shapes of the brains are quite different among the families studied here (Figure 3). The brain of Galbula ruficauda is clearly the most different one in its overall silhouette. Colaptes melanochloros (Figure 4c) has a sub‐rounded or oval shaped brain, without major notches, contrary to the brain of Ramphastos toco (Figure 4d). The brain morphology of Galbulidae clearly separates from the other families’ species. At the present stage it is not prudent to conclude if any of the different characteristics are derived or plesiomorhpic since the only feature that showed a strong phylogenetic signal was the ratio between the optic lobes and the telencephalic hemispheres.

The position of the eminentia sagittalis in the telencephalic hemispheres is variable. It is located more rostrally (type A, Stingelin, 1957) as in G. ruficauda (Figure 8a) or more centrally (type B, Stingelin, 1957) as in Bucconidae (Figures 4b, 8b), Picidae and Ramphastidae (Figures 4c,d, 8c,d). This can also be shown through the ratio between the Wulsts length and telencephalic hemispheres length: the bigger the ratio is, the better the eminentiae sagittales fit in type B. Ramphastos toco is the one with the biggest ratio (in Ramphastidae these structures are longer but thinner), and G. ruficauda with the smallest one (almost half the value of R. toco).

The type of eminentia sagittalis seems to have taxonomic implications (Milner & Walsh, 2009). This may be the case of the set of birds studied here, which separates G. ruficauda (type A) from the rest (type B).

It is well known that the eminentiae sagittales are related to visual and somatosensory inputs (Wild, 2009). This is because the underlying soft‐tissue structure, the hyperpallium, is part of the thalamofugal visual pathway linked to perception of contours, distance discrimination, and spatial orientation among others abilities (Clark & Colombo, 2020; Koshiba et al., 2005). Ramphastos toco has the biggest eminentiae sagittales in relation to the telencephalic length (relative size), contrary to what we expected to find, according to our first hypothesis. Recently, Early et al., 2020b, 2020a,2020b, 2020a demonstrated that eminentiae sagittales size is a good proxy for the underlying visual tissue. Based on this, the eminentiae sagittales’ size may be mainly connected to the huge visual inputs toucans need to process, which is crucial for maneuverability in the trees when distinguishing the fruits they eat, choosing mate (Martin, 2009; Moermond & Denslow, 1985) or avoiding predators (Martin, 2009). Our first hypothesis stated that insectivorous taxa that catch their prey during flight that need precise and fast movements to catch their prey, have well developed eminentiae sagittales compared to fruit eaters; consequently, we predicted that Jacamars and Puffbirds would have larger eminentiae sagittales than woodpeckers and toucans. The observations we have reached so far allow us to reject H1.

It has been proposed that an increase in foliation would represent an increment in cerebellar surface area, which also represents an increase in cerebellar tissue (Striedter, 2005). Similarly, an increment in the degree of cerebellar foliation could also lead to an expansion in the volumes of the cerebellar tissue layers (Cunha et al., 2020). The cerebellum is connected through various pathways to different regions of the brain, particularly the cerebral cortex (Cunha et al., 2020). Much of the variation in the degree of foliation can be attributed to allometric relationships with cerebellar size, brain size, and body size (i.e., larger animals have larger brains with larger, more foliated cerebella; Yopak et al., 2020 and references therein). Thus, we expected to find bigger cerebella, with more visible folia, among Ramphastidae, the largest of the Piciformes studied here. The cerebellum is longer than wider in all specimens except in Picidae where it is as long as it is wide (Table 2). In all specimens, the number of visible folia in the endocast is variable: up to seven in Galbula, four in Nystalus, five in Monasa, four to six in Picidae, and four in Ramphastidae. Our second hypothesis stated that species that require high beak control would show larger cerebellum compared to other brain regions and higher number of visible folia. Therefore, we predicted that toucans that require high precision to move around tree branches to collect primarily fruit will have larger cerebella and more abundant visible folia than woodpeckers. Results achieved here allow the rejection of H2.

Optic lobes ratio relative to the telencephalic hemispheres was the only index that yielded a high phylogenetic signal (K > 1, Table 2). Bucconidae have the largest optic lobes ratio (~74%), almost twice the size of the one in Galbula ruficauda (~39%,). Galbula ruficauda (whose eminentiae sagittales are small) and Picidae present similar ratios (~38%), both being insectivorous taxa; however, both Bucconidae and Galbulidae forage during flight and Picidae do it on the ground. In Ramphastids, the ratio of optic lobes is intermediate (~53%). However, they present the highest eminentia sagittalis ratio of all. In these frugivorous birds, the vision is crucial to select food or maneuver between the trees. In this sense, any functional explanation for the values registered in Ramphastidae could be ruled out. However, the high values of optic lobes ratio of Bucconidae may be explained by the accurate maneuverability needed when foraging during flight. Nevertheless, as stated before, this may be in contradiction with the conclusions achieved based on the smaller wulst's size observed in Bucconidae.

Based on the descriptions and comparisons made so far, it is clear that G. ruficauda is separated from its sister group, the Bucconidae, and in many respects, from the other taxa studied here. In general lines and for all taxa, the following aspects are the most notable ones. Picidae and Ramphastidae have proportionally larger brains. The telencephalic hemispheres are wider than longer in G. ruficauda, Ramphastidae and Bucconidae, but almost as wider as longer in Picidae. Regarding the position of the eminentiae sagittales, G. ruficauda fits in type A, but Bucconidae, Picidae and Rhamphastidae fit into type B. Galbulidae and Bucconidae have small eminentiae sagittales, much smaller than those ones of the Rhamphastidae. The eminentiae sagittales are poorly developed in G. ruficauda. Olfactory bulbs are not an outstanding structure in any of the species studied here. The olfactory ratio varies among 5.5% to 14.3%. Although there is a great variation between species, the highest value does not represent a great proportion of the telencephalic hemisphere length. G. ruficauda shows a proportionally larger cerebellum compared with the rest of the species studied here. The number of the cerebellar folia is variable: Ramphastidae, Nystalus and some Picidae have the lowest number of folia, meanwhile Galbulidae show the highest. Although it has not been studied in much detail, the size of specific folia is reportedly associated with flight behavior (Iwaniuk et al., 2007b; Wylie et al., 2018) and cognitive ability (Sultan, 2005) in birds.

These statements allow us to accept our third hypothesis that states there are marked differences between the brain shape of the four families studied here that could have systematic implications. With more confidence, we establish that Galbula ruficauda is markedly separated from the other taxa studied in the present work.

The bony labyrinth of vertebrates houses the semi‐circular canals. These canals sense rotational accelerations of the head and play a role in gaze stabilization during locomotion (Benson et al., 2017). Stabilization is achieved through two reflexes (the vestibulo‐ocular reflex and vestibulo‐collic reflex), resulting in compensatory movements of the eyes and neck in the opposite sense to head motions. This action avoids blurred vision during locomotion, something particularly important for taxa that rely upon visual clues to navigate cluttered environments, such as forest canopies (Benson et al., 2017). Bucconidae show an anterior semi‐circular canal (ASC) more developed than the rest of the canals (Figure 9B). Some birds such as storks and pelicans (Sipla, 2007) that need constant wing position adjustments during aerial maneuvres, have been reported to have this condition (Pennycuick, 1975; Spear & Ainley, 1997). Presumably, flying insectivores may have this ability. However, Galbula ruficauda is separated from the Bucconidae by having the three canals equally developed (Figure 9a). Also, in toucans, the ASC predominates in size with respect to the other two semi‐circular canals (Figure 9d). In this case, the relationship between the size of a canal could hold a relation with the environment where toucans live. In any case, it is important to highlight that ASC oversizing is frequent among most birds (Sipla, 2007).

Both ASC and horizontal semi‐circular canals (HSC) are well developed in Picidae (Figure 9C). A strong correlation between the HSC and air maneuvrability has been postulated for birds such as Falconiformes, Strigiformes and Apodiformes (Sipla, 2007). In the case of the Picidae, the most plausible explanation is that it is related to stabilization during climbing, or during the action of digging holes for food or building their nests.

Table 3 includes estimates of hearing capacities. The four families showed similar mean hearing capacities (~2462–3317 Hz). The lower limit (~393 Hz for Colaptes pitius) and the upper limit (~6174 Hz for G. ruficauda) were similar across them all. Compared to the limited set of actual measured values available for living birds, the estimates obtained here maintain a generalized range of hearing, without reaching the lowest frequency sensitivity (emus, ~80 Hz) or the highest (barn owls, ~9500 Hz) (Walsh et al., 2009).

5. CONCLUSIONS

Here, three hypotheses were proposed, but only the third hypothesis (there are marked differences between the brain shape of the four families studied here that bring valuable information of this interesting bird group) can be accepted.

The three semi‐circular canals are equally developed only in Galbula but the ASC predominates in size in the remainder families. Nevertheless, mean hearing capacities are similar in the four families (~2462–3317 Hz).

Identifying brain morphological traits associated with functional or ecological abilities have important implications not only to better understanding of the evolutionary implications of certain characteristics but also because they allow identifying phylogenetic or phenotypic relationships with a better degree of confidence. We found that only the ratio of the optic lobes to the telencephalic hemispheres has a phylogenetic signal, so the remainder of the indices would have to be explained independently of inheritance.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

AUTHOR CONTRIBUTIONS

The first and the second author conceived the idea, design and experiment. They also analyzed the data. The first, second and the third author collected the data. The first, second and fourth author wrote the paper. The second and fourth author contributed to substantial resources and funding.

ACKNOWLEDGMENTS

The authors thank Ricardo Torres y Mario Cabrera (MZUC) for the loan of material. The authors also thank the Editor Anthony Graham and two anonymous reviewers for their helpful comments and suggestions. Additionally, the authors thank professor Andrea Martin for the English corrections. Finally, the authors thank CONICET, for permanent support. This study was funded by PICT 2330 and PIP 0437 to CPT, PICT 1319 to FJD, and PUE 2016—CONICET—CICTERRA.

DATA AVAILABILITY STATEMENT

The data can be requested to THE corresponding author.

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