Research Article |
Corresponding author: Daniela A.S. Bôlla ( danielabolla@hotmail.com ) Academic editor: Ricardo Moratelli
© 2020 Fernando Carvalho, Daniela A.S. Bôlla, Viviane Mottin, Suelen Zonta Kiem, Jairo J. Zocche, Fernando C. Passos.
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:
Carvalho F, Bôlla DAS, Mottin V, Kiem SZ, Zocche JJ, Passos FC (2020) Chilling to the bone: Lower temperatures increase vertebrate predation by Tonatia bidens (Chiroptera: Phyllostomidae). Zoologia 37: 1-5. https://doi.org/10.3897/zoologia.37.e37682
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The greater round-eared bat, Tonatia bidens (Spix, 1823), is a medium-sized phyllostomid bat distributed in the north of Argentina, Paraguay and Brazil. The diet and foraging patterns of this species are poorly known. We analyzed the composition of the diet of a population of T. bidens and how the temperature influences the consumption of vertebrates and invertebrates. To describe diet composition, we conducted weekly collections of food scrap from two monospecific night-perches. Data of temperature for the study period were taken from the meteorological station installed 300 m from the collection perches. The influence of temperature was evaluated using generalized linear models (GLMs) with negative binomial distribution. Tonatia bidens consumed 28 taxons (204 records), being at least 17 Artropods and 11 Passeriformes birds. Temperature explained a greater proportion of vertebrate abundance (R2 = 0.23) than invertebrate (R2 = 0.16) or to both pooled (R2 = 0.11). The relation with temperature was positive with invertebrates and negative with the vertebrates. The diet of the population of T. bidens comprised mainly invertebrates, which were the most frequent and diverse taxa. Data suggests that T. bidens has a diverse diet, with proportion of the item’s consumption varying temporally. Environmental factors, such as the temperature presented on this work, seems to be good proxies for the dietary traits of this species.
Atlantic Forest, bat diet, diet seasonality, invertebrate predation, trophic guild
The greater round-eared bat Tonatia bidens (Spix, 1823) is a medium size phyllostomid bat distributed in the North of Argentina, Paraguay and Brazil (
The diet of T. bidens is mainly composed of invertebrates from the Orders Lepidoptera, Coleoptera, Blattodea, Orthoptera and Hemiptera (
The diet of T. bidens is known only for a few localities, making it difficult to evaluate the trophic ecology of this species. In Brazil, there are records of T. bidens in 12 states (
The diet of T. bidens is primarily based on small living animals. Since the availability of these potential resources change temporally, we hypothesize that the diet of T. bidens changes according to the known seasonal variations in their availability, mainly invertebrates (
We sampled bats’ roosts at Reserva Particular do Patrimônio Natural (RPPN) Salto Morato (25°10’27”S; 48°17’49”W), located in the Guaraqueçaba municipality, Northern coast of Paraná, southern Brazil (Fig.
The RPPN Salto Morato is part of the largest continuous remnant of the Atlantic Forest biome, which covers 22.53 km2. This reserve is inserted in the Environmental Protection Area of Guaraqueçaba (APA de Guaraqueçaba –
To describe the composition of the diet of T. bidens, we performed weekly collections of food scrap in two monospecific night-perches between March 2013 and November 2013. These perches were located externally to the roof of the buildings and lodgings for visitors of the RPPN Salto Morato. In each of the perches we manually collected all food scraps left by the bats, which were allocated in plastic bags identified with month.
In the lab, samples were examined, and food items were identified to the lowest possible taxonomic level. We used the keys of
The food items of T. bidens were described according to the richness and frequency of the food items, and the number of items. We considered the total number of taxons observed in each sample (pool of four weekly collections) as a measure of richness for each sampled month. We categorized the items frequency according to the Constancy Index (C), which separates the frequency (number of samples of the studied taxon divided by the total number of samples) into three categories: Rare – less than 25%, Uncommon – from 26% to 50% and, Frequent – present in more than 50% of the samples. To determine the number of the items (abundancy) we used the protocol described by
The influence of temperature on the food items consumed by T. bidens was evaluated using generalized linear models (GLMs) with negative binomial distribution due to the over dispersion of the data. For the analyses, the response variables were number of records of: invertebrates (“abundance of invertebrates” from now on), vertebrates (“abundance of vertebrates” from now on) or vertebrates and invertebrates pooled (“total abundance” from now on). We used monthly temperature averages as a predictor variable. All analyses were performed in the software R version 3.4.2, using the “MASS” package.
Tonatia bidens
consumed specimens of 28 taxons (204 records), at least 17 of which were Artropods and 11 were Passeriform birds (Table
Temperature explained a greater proportion of vertebrate abundance variation (R2 = 0.23) than invertebrate (R2 = 0.16) or both pooled (R2 = 0.11), and the relationship of temperature with invertebrates was positive, being negative with vertebrates (Fig.
List of taxons, monthly abundance, total (AB) and frequency (FR) of the occurrence of the items consumed by Tonatia bidens in Atlantic Forest environment, in northern coast of Paraná State, southern of Brazil.
Taxons | Sampling months | AB | FR | ||||||||
M | A | M | J | J | A | S | O | N | |||
Vertebrates | |||||||||||
Passeriformes | |||||||||||
Onychorhynchidae | |||||||||||
Myiobius sp. | 1 | 1 | 11.1 | ||||||||
Parulidae | |||||||||||
Basileuterus culicivorus | 1 | 1 | 11.1 | ||||||||
Rhynchocyclidae | |||||||||||
Leptopogona maurocephalus | 1 | 1 | 11.1 | ||||||||
Phylloscartes oustaleti | 1 | 1 | 11.1 | ||||||||
Rhynchocyclidae | |||||||||||
Rhynchocyclidae sp. | 2 | 1 | 3 | 22.2 | |||||||
Thraupidae | |||||||||||
Tangara seledon | 1 | 1 | 2 | 22.2 | |||||||
Troglodytidae | |||||||||||
Troglodytes musculus | 2 | 1 | 1 | 4 | 33.3 | ||||||
Passeriformes sp. | 1 | 1 | 1 | 1 | 1 | 5 | 55.6 | ||||
Apodiformes | |||||||||||
Apodiformes sp. | 2 | 1 | 1 | 4 | 33.3 | ||||||
Trochilidae | |||||||||||
Thalurania glaucopis | 1 | 1 | 1 | 3 | 33.3 | ||||||
Trochilidae sp. | 1 | 1 | 1 | 1 | 4 | 44.4 | |||||
Invertebrates | |||||||||||
Blattodea | |||||||||||
Blattidae | 3 | 6 | 2 | 1 | 1 | 1 | 1 | 1 | 16 | 88.9 | |
Blattodea sp. | 2 | 2 | 1 | 5 | 33.3 | ||||||
Coleoptera | |||||||||||
Cerambycidae | 4 | 3 | 1 | 3 | 3 | 2 | 16 | 66.7 | |||
Scarabaeidae | 1 | 1 | 1 | 3 | 33.3 | ||||||
Coleoptera sp. | 8 | 3 | 5 | 1 | 1 | 5 | 23 | 66.7 | |||
Hemiptera | |||||||||||
Cicadidae | 2 | 2 | 1 | 5 | 33.3 | ||||||
Hemiptera sp. | 1 | 1 | 11.1 | ||||||||
Lepidoptera | |||||||||||
Erebidae | 1 | 1 | 1 | 3 | 33.3 | ||||||
Geometridae | 1 | 1 | 11.1 | ||||||||
Hepialidae | 1 | 1 | 2 | 22.2 | |||||||
Noctuidae | 2 | 2 | 11.1 | ||||||||
Nymphalidae | 1 | 1 | 2 | 22.2 | |||||||
Sphingidae | 2 | 8 | 8 | 6 | 24 | 44.4 | |||||
Lepidoptera sp. | 3 | 4 | 2 | 1 | 5 | 1 | 1 | 2 | 19 | 88.9 | |
Orthoptera | |||||||||||
Gryllidae | 3 | 3 | 11.1 | ||||||||
Tettigoniidae | 5 | 5 | 7 | 1 | 1 | 1 | 3 | 23 | 77.8 | ||
Orthoptera sp. | 8 | 7 | 1 | 1 | 2 | 1 | 1 | 4 | 2 | 27 | 100 |
Total records | 42 | 47 | 33 | 9 | 23 | 9 | 16 | 18 | 7 | 204 |
The population of T. bidens analyzed consumed mainly invertebrates, which were the most frequent and diverse taxons. Contrary to our hypothesis, temperature explained the consumption of vertebrates better than the consumption of invertebrates, even though there was a greater consumption of Arthropods between May and August. This latter pattern can be due to the lower abundance of Arthropods on cold periods (
Cockroaches were consumed in greater numbers among the invertebrate, when compared with moths and beetles. This is inconsistent with the other studies’ results, which found that Coleoptera and Lepidoptera were the most frequently consumed items in T. bidens diet (see
The high richness (41% of all the taxons consumed) and frequency of occurrence (at least a record in each sample) of birds in the diet of T. bidens indicates that this food item is an important resource for the species. In other areas of Atlantic Forest, T. bidens was recorded preying on 75 individuals of 28 bird species (
Data obtained in the South and Southeast portions of the Atlantic Forest suggest that the diet of T. bidens varies temporally (e.g.,
Based on the results of our work and on other studies on the species, we suggest that T. bidens is embedded in the Omnivores guild, since guild classifications do not account for seasonal variations and a more general classification (such as omnivorous) solves the disagreement among the previous trophic classifications (e.g.,
As observed for other Neotropical bats, the knowledge about the ecological and biological attributes of T. bidens is limited, which classifies this species as “insufficient data” on endangered species’ lists (Barquez e Díaz 2016). In the state of Paraná, more specifically, this species is included in the Conservation Plan for Threatened Mammal Species (Plano de Conservação para Espécies de Mamíferos Ameaçados, in Portuguese) which indicated the necessity of studies on its biology and ecology (
Many thanks to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the master scholarship awarded by D.A.S. Bôlla (process 131784/2017-0), to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the doctorate scholarship awarded by V. Mottin (process 88887.343525/2019-00), to Thuany S. Machado for the samples sorting and identification in the lab, and also to the RPPN Salto Morato workers for the support in fieldwork activities. This work was supported by the Fundação Boticário de Proteção a Natureza under Grant [0105-20112-BR] and Fundação de Amparo a Pesquisa e Inovação do Estado de Santa Catarina under Grant [2017TR1706].