Research Article |
Corresponding author: Raul F.D. Sales ( raulsales17@gmail.com ) Academic editor: Fabricius Domingos
© 2020 Jaqueiuto S. Jorge, Raul F.D. Sales, Roberto L. Santos, Eliza M.X. Freire.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Jorge JS, Sales RFD, Santos RL, Freire EMX (2020) Living among thorns: herpetofaunal community (Anura and Squamata) associated to the rupicolous bromeliad Encholirium spectabile (Pitcairnioideae) in the Brazilian semi-arid Caatinga. Zoologia 37: 1-12. https://doi.org/10.3897/zoologia.37.e46661
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Bromeliads are important habitats for reptiles and amphibians, and are constantly used as shelter, refuge, foraging or thermoregulation sites due to their foliar architecture, which allows for constant maintenance of humidity and temperature. This study aimed to identify the herpetofauna inhabiting the non-phytotelmata rupicolous bromeliad Encholirium spectabile Mart. ex Schult. & Schult.f. and to analyze the microhabitat usage of these bromeliads by different species in the Caatinga of northeastern Brazil. From January 2011 to August 2012, we collected data by active search throughout three paralel transects in a rock outcrop in the municipality of Santa Maria, state of Rio Grande do Norte. We recorded four species of anuran amphibians, six lizards, and seven snakes in the bromeliads. The average air temperature was lower and air humidity higher inside than outside the bromeliads, and bromeliads at the rock outcrop borders had lower temperatures and higher humidity than those at the center. We found a significant difference in the distribution of individuals throughout the rock outcrop, with most specimens found at the borders. We also found significant differences regarding the use of each microhabitat by the taxonomic groups, with lizards and snakes using green leaves and dry leaves evenly, along with fewer records in inflorescence stems, and anurans mainly using green leaves, with few records on dry leaves, and no records in the inflorescence stems. This study highlights rupicolous bromeliads as key elements in the conservation and maintenance of amphibians and reptiles in the rock outcrops of Brazilian semi-arid Caatinga.
Amphibians, associated fauna, Bromeliaceae, habitat use, reptiles
The Bromeliaceae family is characterized by terrestrial, epiphytic or rupicolous plants which have simple leaves organized in rosette shapes. Bromeliads are often used by animals as shelter to avoid excessive sun exposure or as a refuge against predators, due to their foliar architecture which enables relatively constant maintenance of internal humidity and temperature, creating a less stressful microhabitat when compared to the external environment (
Among vertebrates, anuran amphibians comprise the taxa most intimately associated to bromeliads, and have developed very unique relationships with these plants (
Regarding reptiles, information about their interactions with bromeliads is still scarce. Available data in South America consists of a few autoecological studies with some lizard species or studies that investigated the whole herpetofauna inhabitant of a single bromeliad species (
Pitcairnioideae
bromeliads of the Encholirium genus, popularly known as “macambiras-de-flecha” (arrow macambiras), are endemic to Brazil and occur in rock outcrops of the Caatinga and Cerrado regions. This genus presents a high diversity in the Cadeia do Espinhaço rock fields in the state of Minas Gerais, with exception of Encholirium spectabile Mart. ex Schult. & Schult.f., which occurs throughout the Caatinga in northeastern Brasil, and also in transitional areas between Caatinga and Atlantic Forest (
Despite the remarkable abundance of E. spectabile patches in the semi-arid Brazilian Caatinga, and their potential as microhabitat for the herpetofauna, they have constituted poorly sampled habitats in previous studies with herpetofauna in this region, despite the local occurrence of these bromeliads in the study sites (e.g.
This study was conducted at Fazenda Tanques (5.853°S, 35.701°W; datum WGS84, 137 m above sea level), in the municipality of Santa Maria, state of Rio Grande do Norte, Brazil (Fig.
Location of the rock outcrop where this study was conducted at Fazenda Tanques, municipality of Santa Maria, Rio Grande do Norte state, northeastern Brazil. The colored lines indicate the transects covered for data collection during the study. Red line: north border transect (T1); yellow line: center transect (T2); green line: south border transect (T3).
The fieldwork was carried out in a large granite rock outcrop (5.855°S, 35.702°W; datum WGS84, 137 m asl) with around 5.8 ha (Fig.
We sampled the rock outcrop monthly from January 2011 to August 2012, with a total of 360 hours of sample effort. Search and data collection occurred throughout three paralel transects of 12 m width and about 1500 m length, situated on the north border (T1), the center (T2) and on the south border (T3) of the outcrop (Fig.
The registered specimens were manually collected whenever possible (most cases), packed in plastic bags and identified with field numbers. In the lab, they were euthanized by cooling followed by freezing (
Herpetofauna species recorded in patches of the rupicolous bromeliad Encholirium spectabile at Fazenda Tanques, municipality of Santa Maria, Rio Grande do Norte, Brazil, from January 2011 to August 2012. N: number of specimens, F: relative frequency (%); microhabitats – GL: Green Leaf, DL: Dry Leaf, IS: Inflorescence Stem.
Taxon | N | F | Microhabitats | Voucher numbers | ||
Anura /Hylidae | DL | GL | IS | |||
Boana raniceps (Cope, 1862) | 10 | 5.2 | 1 | 9 | – | UFRN 2888, 3356-3358 |
Dendropsophus nanus (Boulenger, 1889) | 5 | 2.6 | – | 5 | – | UFRN 3669-3672 |
Scinax x-signatus (Spix, 1824) | 5 | 2.6 | 1 | 4 | – | UFRN 3368-3372 |
Anura /Phyllomedusidae | ||||||
Pithecopus nordestinus (Caramaschi, 2006) | 7 | 3.6 | – | 7 | – | UFRN 2654, 3073, 3839 |
Squamata /Gekkonidae | ||||||
Hemidactylus agrius Vanzolini, 1978 | 28 | 14.5 | 9 | 11 | 8 | UFRN 3354-3364 |
Squamata /Mabuyidae | ||||||
Psychosaura agmosticha (Rodrigues, 2000) | 62 | 32.1 | 4 | 58 | – | UFRN 2882-2883, 2933, 3765, 3925-3930 |
Squamata /Phyllodactylidae | ||||||
Gymnodactylus geckoides Spix, 1825 | 12 | 6.2 | 11 | 1 | – | UFRN 2932, 5509 |
Phyllopezus pollicaris (Spix, 1825) | 4 | 2.1 | 1 | 2 | 1 | UFRN 2935, 3031, 3156 |
Squamata /Tropiduridae | ||||||
Tropidurus hispidus (Spix, 1825) | 9 | 4.7 | 7 | 2 | – | UFRN 3020-3028 |
Tropidurus semitaeniatus (Spix, 1825) | 34 | 17.6 | 30 | 4 | – | UFRN 2934, 3043, 3162, 3762, 3835-3845, 3157-3159 |
Squamata /Boidae | ||||||
Epicrates assisi Machado, 1945 | 4 | 2.1 | 2 | 2 | – | UFRN 3764-3765 |
Squamata /Colubridae | ||||||
Leptodeira annulata (Linnaeus, 1758) | 1 | 0.5 | – | 1 | – | UFRN 5233 |
Lygophis dilepis Cope, 1862 | 1 | 0.5 | – | 1 | – | UFRN 3150 |
Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854 | 4 | 2.1 | 2 | 2 | – | UFRN 3120, 5222-5223 |
Philodryas olfersii (Lichtenstein, 1823) | 3 | 1.6 | 1 | 1 | 1 | UFRN 3364-3366 |
Thamnodynastes almae Franco & Ferreira, 2003 | 3 | 1.6 | 2 | 1 | – | UFRN 3777-3778 |
Thamnodynastes phoenix Franco, Trevine, Montingelli & Zaher, 2017 | 1 | 0.5 | 1 | – | – | UFRN 3044 |
Total individuals | 193 | 100 | 72 | 111 | 10 |
We ramdomly selected 90 bromeliad patches to evaluate the occurrence of differences in air temperature and humidity inside and outside the bromeliads and between border and center bromeliads: 30 on the north border, 30 on the south border and 30 in the center of the rock outcrop. External air temperature and humidity were measured at 1.5 m height above the bromeliad patch, and internal air temperature and humidity in the most central bromeliad of the patch, 5 cm above the rosette center using a digital thermohygrometer (0.1 °C precision; Instrutherm® model HTR-350) with an external sensor attached (Instrutherm® model S-02K). We used independent t-tests to evaluate differences between average air temperatures and humidity inside and outside the bromeliads, as well as to compare bromeliads located at the borders and the center of the outcrop regarding these aforementioned variables.
The two-tailed χ2 test (Chi-squared test –
Microhabitat usage in the bromeliads by the amphibian and reptile species was analyzed. We previously identified that E. spectabile patches are composed of three main microhabitats: 1) Green leaves (living bromeliad leaves), 2) dry leaves (dead leaves usually situated in the base of the bromeliad), and 3) inflorescence stems. We used a loglinear analysis using the chi-squared test as the basis to analyze the different microhabitats usage of bromeliads by anuran amphibians, lizards and snakes. This analysis enables analyzing categorical data with more than two variables, constructing the interaction between such variables. The significance level assumed in all tests was 0.05.
We recorded 17 species of the herpetofauna inhabiting the rupicolous bromeliads (E. spectabile) at Fazenda Tanques: four anuran amphibians, six lizards, and seven snakes (Figs
Lizard species registered in Encholirium spectabile patches at Fazenda Tanques, municipality of Santa Maria, Rio Grande do Norte, Brazil: (10) Psychosaura agmosticha; (11) Hemidactylus agrius; (12) Gymnodactylus geckoides; (13) Phyllopezus pollicaris; (14) Tropidurus hispidus; (15) Tropidurus semitaeniatus.
The bromeliad usage rates by the herpetofauna on the rock outcrop borders and center revealed that the bromeliad patches located on the borders were more frequently used than the bromeliads located in the center (χ2 = 7.02, df = 1, p = 0.003). There were differences regarding the species distribution on the north border and the center (Kolmogorov-Smirnov, Dmax = 0.343, p < 0.001), and the south border and the center (Kolmogorov-Smirnov, Dmax = 0.421, p < 0.001). There was also a significant difference between the south and north borders (Kolmogorov-Smirnov, Dmax = 0.249, p < 0.001), with most specimens registered on the north border. The species that most used the center of the rock outcrop were P. agmosticha (40%) and T. semitaeniatus (37%) lizards. All anuran specimens were found in bromeliads located at the borders, with a distance less than fifteen meters from the surrounding vegetation of the rock outcrop. Except for Epicrates assisi Machado, 1945, all other snake species were only found in the borders.
The average air temperature inside the bromeliads (32.5 ± 1.3 °C, range: 29.9–34.8) was significantly lower than the average air temperature outside the bromeliads (35.5 ± 1.2 °C, range: 32.2–38.9; t = -5.139, df = 29, p = 0.003). Air humidity was higher inside (68.5 ± 1.2%, range: 59.2–79.0) than outside the bromeliads (50.9 ± 1.1%, range: 42.3–61.0), also with a significant difference (t = -4.172, df = 29, p = 0.003). In addition, the bromeliads of the borders had lower temperatures (28.7 ± 1.7 °C, range: 26.5–31.4) than those of the center of the rock outcrop (33.1 ± 1.5 °C, range: 29.9–34.8; t = -3.263, df = 29, p = 0.009), and air humidity was higher in the bromeliads of the borders (70.3 ± 1.5%, range: 58.0–79.1) than those in the center of the rock outcrop (56.3 ± 1.4%, range: 42.1–75.3; t = -3.146, df = 29, p = 0.003).
The loglinear analysis showed significant differences regarding the use of each microhabitat by the taxonomic groups (χ2 = 16.363, df = 4, p = 0.003; Likelihood Ratio = 20.121, df = 4, p < 0.001). Lizards mainly used green leaves (52.3%) and dry leaves (41.6%), with fewer records in inflorescence stems (6.1%). Similarly, snakes mainly used green leaves (47.1%) and dry leaves (47.1%), with only one record in inflorescence stems (5.9%). Anurans used mainly green leaves (92.6%), with few records on dry leaves (7.4%), and no records in inflorescence stems (Table
We registered four anuran amphibian species and thirteen squamate reptile species associated to E. spectabile during this study, which corresponds to 17.4% of amphibians and 31% of reptiles registered for the entire study site, also including other habitats (JSJ unpublished data). Most of these species were also recorded in other sites of the Caatinga region (e.g.
In the case of amphibians, the bromeliad patches were usually close to natural water bodies formed by water accumulating from rains in rock depressions. All anuran species recorded during this study were protecting themselves from sunlight during the day, or in foraging or vocalization activities during the night, which reinforces the hypotheses of the bromeliads acting as foraging site and also shelter from the sunlight, as reported for phytotelmata bromeliads (
Bromeliads provide relatively higher humidity than the external environment because they can retain water in their leaf axils, as well as forming a shaded region due to their foliar architecture (
The lizard species recorded in E. spectabile during this study are similar to the families and genera recorded for tank bromeliads in other Brazilian ecosystems, demonstrating a tendency towards the use of bromeliads by these taxa (
A similar pattern was found for snakes, because the richness found in this study is very similar to that found in studies with tank bromeliads. Lygophis dilepis Cope, 1862, Oxyrhopus petola Linnaeus, 1758, Philodryas olfersii (Lichtenstein, 1823) and Thamnodynastes cf. pallidus were recorded in restingas of Rio de Janeiro state, southeastern Brazil, using bromeliads as a foraging site (
With respect to the use of microhabitats of E. spectabile by the herpetofauna, dry leaves, usually situated in the base of the bromeliads, seem to be used mainly as shelter from predators; for instance, lava lizards (T. hispidus and T. semitaeniatus), which used mainly this microhabitat (Table
Encholirium
deserves more prominence in the national conservation policies, not only because it is endemic to Brazil, which in itself should already guarantee special attention, but because it is vulnerable to extinction. According to
This study was supported by research grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico to JSJ (process 130363/2014-6) and EMXF (process 313661/2017-0) and from Coordernação de Aperfeiçoamento de Pessoal de Nível Superior to RFDS (process 1558610). We also thank the employees of the Fazenda Tanques through Mr Toinho for their support in the field and to all others who helped by contributing feedback to improve the manuscript. We also thank two anonymous reviewers for helpful comments on the manuscript.