Abstract

This study aimed to analyze the diet and trophic niche breadth of an insectivorous bat very common in an urban environment in southern Brazil. To analyze the feeding habit of Molossus rufus, it was necessary to collect fecal samples in urban colonies in the city of Maringá, State of Paraná. Samplings occurred from November 2018 to September 2019, including rainy and dry seasons. The fragments found in the samples were identified up to the level of order or family whenever possible. Percentage of volume and frequency of occurrence, Feeding Index (IAi%), PERMANOVA, and trophic niche breadth were used. Thus, a total of 140 samples were obtained, 92 for the rainy season and 48 for the dry season. In terms of percentage of volume, the diet consisted mainly of Hymenoptera (46.9%) in the rainy season and Coleoptera (39.2%) in the dry season. The results for standardized trophic niche breadth were Ba = 0.36 for the rainy season and Ba = 0.37 in the dry season, indicating a low food diversity. In conclusion, there was a food preference on the part of M. rufus according to the season evaluated, with Hymenoptera and Coleoptera being the most relevant dietary items.

Key words
Bat; insectivory; feeding habits; seasonality; southern Brazil

INTRODUCTION

The degradation of the natural environment has caused changes in the habitats and behavior of wild species (Ellington & Gehrt 2019ELLINGTON EH & GEHRT SD. 2019. Behavioral responses by an apex predator to urbanization. Behav Ecol 30(3): 821-829., Frick et al. 2020FRICK WF, KINGSTON T & FLANDERS J. 2020. A review of the major threats and challenges to global bat conservation. Ann N Y Acad Sci 1469(1): 5-25., Lynch et al. 2021LYNCH L, KANGAS M, BALLUT N, DOUCET A, SCHOENECKER K, JOHNSON P, GHAREHAGHAJI M & MINOR ES. 2021. Changes in Land Use and Land Cover Along an Urban-Rural Gradient Influence Floral Resource Availability. Curr Landsc Ecol Rep 6: 46-70.). Several mammals in Brazil are present in urban areas; this is possible because they have adapted to the urban environment (Pacheco et al. 2010PACHECO SM, SODRÉ M, GAMA AR, BREDT A, SANCHES EMC, MARQUES RV, GUIMARÃES MM & BIANCONI G. 2010. Morcegos urbanos: Status do conhecimento e plano de ação para a conservação no Brasil. Chirop Neotrop 16(1): 629-647.). Bats use shelters in urban constructions, such as roofs or abandoned buildings, since the destruction of natural shelters, such as caves and forests, has become frequent with the advance of urbanization (Pacheco et al. 2010PACHECO SM, SODRÉ M, GAMA AR, BREDT A, SANCHES EMC, MARQUES RV, GUIMARÃES MM & BIANCONI G. 2010. Morcegos urbanos: Status do conhecimento e plano de ação para a conservação no Brasil. Chirop Neotrop 16(1): 629-647.).

In urban centers, there are several species of insectivorous bats. Usually, these animals consume a variety of arthropods that birds cannot prey on because they have nocturnal habits, and most birds are diurnal (Reis et al. 2017REIS NR, PERACCHI AL, BATISTA CB, LIMA IP & PEREIRA AD. 2017. História natural dos morcegos brasileiros: chave de identificação de espécies, 1a ed. Rio de Janeiro: Technical Books Editora, 416 p.). Bats present different foraging strategies, for example, vespertilionids and emballonurids obtain most of their food in mid-flight, capturing insects up to the approximate height of the treetops, whereas molossids generally perform their foraging above this stratum (Reis et al. 2007REIS NR, PERACCHI AL, PEDRO WA & LIMA IP. 2007. Morcegos do Brasil. Londrina: Nélio R. dos Reis, 253 p.). How these animals perform the foraging and the types of habitats occupied can indicate, in a considerable way, the composition of the diet (Emiliano et al. 2017EMILIANO SB, PEREIRA LA, PRESSINATTE JR S & MIRANDA JMD. 2017. Dieta de morcegos insetívoros (Mammalia: Chiroptera) em fragmentos de Floresta de Araucárias, no Sul do Brasil. Rev Bras Zoociências 18(3): 187-196.).

Many insects are urban pests and possible vectors of infectious agents. In common with frugivorous bats playing an important role in seed dispersal, as demonstrated in Faustino et al. (2021)FAUSTINO CL, DIAS RM, FERREIRA SR & ORTÊNCIO-FILHO H. 2021. Frugivorous bat (Chiroptera: Phyllostomidae) community structure and trophic relations in Atlantic Forest fragments. Acta Sci Biol Sci 43(1): e52030. and Jacomassa et al. (2021)JACOMASSA FAF, BERNARDI IP & PASSOS FC. 2021. Seasonal diet variation, preferences and availability of resources consumed by Sturnira lilium (É. Geoffroy St.-Hilaire, 1810) (Chiroptera: Phyllostomidae) in Brazilian seasonal deciduous forest. An Acad Bras Cienc 93: e20201571., insectivorous bats are relevant because they consume insects in abundance. One of the important ecosystem services provided by insectivorous bats is the regulation function, which means suppressing the abundance of these arthropods in a given environment and acting on effective biological pest control (Boyles et al. 2011BOYLES JG, CRYAN PM, MCCRACKEN GF & KUNZ TH. 2011. Economic importance of bats in agriculture. Science 332(6025): 41-42., Cleveland et al. 2006CLEVELAND CJ ET AL. 2006. Economic value of the pest control service provided by Brazilian free-tailed bats in south-central Texas. Front Ecol Environ 4(5): 238-243.). Certain species of insectivorous bats can consume insects in an amount equivalent to their body weight in just one night (Reis et al. 2017REIS NR, PERACCHI AL, BATISTA CB, LIMA IP & PEREIRA AD. 2017. História natural dos morcegos brasileiros: chave de identificação de espécies, 1a ed. Rio de Janeiro: Technical Books Editora, 416 p.). This means that large numbers of individuals in food activity contribute to the removal of thousands of insects from the environment per night (Reis et al. 2017REIS NR, PERACCHI AL, BATISTA CB, LIMA IP & PEREIRA AD. 2017. História natural dos morcegos brasileiros: chave de identificação de espécies, 1a ed. Rio de Janeiro: Technical Books Editora, 416 p., Kurta et al. 1989KURTA A, BELL GP, NAGY KA & KUNZ TH. 1989. Energetics of pregnancy and lactation in freeranging little brown bats (Myotis lucifugus). Physiol Zool 62(3): 804-818.).

These animals have a high potential to control agricultural pests, which Lepidoptera, Hemiptera, and Coleoptera are some of the main orders of insects that cause losses in agriculture (Williams-Guillén et al. 2008WILLIAMS-GUILLÉN K, PERFECTO I & VANDERMEER J. 2008. Bats limit insects in a neotropical agroforestry system. Science 320(5872): 70., Leelapaibul et al. 2005LEELAPAIBUL W, BUMTUNGSRI S & PATTANAWAIBOON A. 2005. Diet of wrinkle-lipped free-tailed bat (Tadarida plicata Buchannan, 1800) in central Thailand: insectivorous bats potentially act as biological pest control agents. Acta Chiropt 7(1): 111-119.). However, these insects are also common in urban areas, as observed in Garcia (2007)GARCIA AH. 2007. Levantamento, identificação e avaliação dos danos de insetos em árvores ornamentais na área urbana de Goiânia (GO). Pesq Agropec Trop 29(1): 77-81.. Some insect species can be disease vectors (Papavero & Guimarães 2000PAPAVERO N & GUIMARÃES JH. 2000. The taxonomy of brazilian insects vectors of transmissible diseases (1900-2000) - Then and Now. Mem Inst Oswaldo Cruz 95(1): 109-118.) and insectivorous bats can be essential to reduce their population in cities. Some Diptera, for example, are transmitters of important public health pathogens, such as Aedes aegypti, a vector of dengue and yellow fever viruses (Galati et al. 2015GALATI EAB, CAMARA TNL, NATAL D & CHIARAVALLOTI-NETO F. 2015. Mudanças climáticas e saúde urbana. Rev USP (107): 79-90.). There is evidence that the occurrence of these insects may be seasonal (Vasconcellos et al. 2010VASCONCELLOS A, ANDREAZZE R, ALMEIDA AM, ARAUJO HFP, OLIVEIRA ES & OLIVEIRA U. 2010. Seasonality of insects in the semi-arid Caatinga of northeastern Brazil. Rev Bras Entomol 54(3): 471-476.), which indicates the possibility of seasonality also in the food consumption of insectivorous bats.

The availability of food resources in the environment, at different times of the year, maybe related to rainfall, because, according to Barclay (2008)BARCLAY E. 2008. Is climate change affecting dengue in the Americas? The Lancet 371(9617): 973-974., the increase in the volume of rain or temperature can affect the spatial and temporal distribution of insects. In this way, it becomes relevant to evaluate the trophic niche breadth of bats relative to seasonality.

Molossus rufus É. Geoffroy, 1805 is one of the most common insectivorous species found in an urban environment in Brazil. These Molossidae bats are known as acrobatic bats, given their ability to perform maneuvers during flight (Gregorin & Taddei 2002GREGORIN R & TADDEI VA. 2002. Chave artificial para a identificação de molossídeos brasileiros (Mammalia, Chiroptera). J Neotrop Mammal 9(1): 13-32., Nolte et al. 2009NOLTE MJ, HOCKMAN D, CRETEKOS CJ, BEHRINGER RR & RASWEILER IV JJ. 2009. Embryonic staging system for the Black Mastiff bat, Molossus rufus (Molossidae), correlated with structure-function relationships in the adult. Anat Rec 292(2): 155-168.). They are large bats, with a body mass from 21 to 43 g and forearms from 46 to 53 mm long (Gregorin & Taddei 2002GREGORIN R & TADDEI VA. 2002. Chave artificial para a identificação de molossídeos brasileiros (Mammalia, Chiroptera). J Neotrop Mammal 9(1): 13-32., Reis et al. 2017REIS NR, PERACCHI AL, BATISTA CB, LIMA IP & PEREIRA AD. 2017. História natural dos morcegos brasileiros: chave de identificação de espécies, 1a ed. Rio de Janeiro: Technical Books Editora, 416 p.). Food habit records include orders such as Coleoptera, Hymenoptera, Hemiptera, Orthoptera, Lepidoptera, Diptera, Odonata (Fenton et al. 1998FENTON MB ET AL. 1998. Emergence, echolocation, diet and foraging behavior of Molossus ater (Chiroptera: Molossidae). Biotropica 30(2): 314-320., Freeman 1981FREEMAN PW. 1981. A multivariate study of the Family Molossidae (Mammalia, Chiroptera): Morphology, ecology, evolution. Fieldiana Zool 7: 1-173., Marques 1986MARQUES SA. 1986. Activity cycle, feeding and reproduction of Molossus ater (Chiroptera: Molossidae) in Brazil. Bol Mus Para Emilio Goeldi Ser Zool 2(2): 159-179., Howell & Bruch 1974HOWELL DJ & BRUCH D. 1974. Food habits of some Costa Rican bats. Rev Biol Trop 1(2): 281-294., Pine 1969PINE RH. 1969. Stomach contents of a Free-Tailed bat, Molossus ater. J Mammal 50(1): 162.), and for southern Brazil, Emiliano et al. (2017)EMILIANO SB, PEREIRA LA, PRESSINATTE JR S & MIRANDA JMD. 2017. Dieta de morcegos insetívoros (Mammalia: Chiroptera) em fragmentos de Floresta de Araucárias, no Sul do Brasil. Rev Bras Zoociências 18(3): 187-196. reported high consumption of Coleoptera and Lepidoptera by Molossus spp.

Few studies describe the diet of tropical insectivorous bats. Thus, the goal of this study was to describe the diet and the trophic niche breadth of M. rufus in a tropical urban environment in southern Brazil, taking into account the seasonality and to understand the importance of M. rufus in the suppression of insects that can cause some damage to society’s lifestyle.

MATERIALS AND METHODS

Study area

Sampling was conducted in six urban shelters for insectivorous bats in Maringá (23°25’16.12” S, 51°55’59.16” W), municipality of the State of Paraná, Southern Brazil, from November 2018 to September 2019. The area was located within the boundaries of the Atlantic Forest; the type of vegetation in the municipality is Semideciduous Seasonal Forest (Instituto Brasileiro de Geografia e Estatística [IBGE] 2004IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. 2004. Mapa de vegetação do Brasil. Rio de Janeiro.). The climate, according to the Köppen classification, is Cfa, subtropical mesothermal, humid, without a rigorous dry season, and with hot summers (Maack 2012MAACK R. 2012. Geografia Física do Estado do Paraná, 4a ed. Curitiba: Ed. UEPG, 526 p.).

In the study area, the dry season was from April to September 2019, with the lowest rainfall in August (5.6 mm); and the highest rainfall volumes from November 2018 to March 2019, peaking in March (153.2 mm), (Figure 1) (data provided by the Sistema de Tecnologia e Monitoramento Ambiental do Paraná [SIMEPAR] 2020).

Figure 1
Ombrothermic diagram for a tropical urban environment in southern Brazil, from November 2018 to September 2019 (SIMEPAR 2020SIMEPAR - SISTEMA DE TECNOLOGIA E MONITORAMENTO AMBIENTAL DO PARANÁ. 2020. Maringá (PR).).

Sampling

For both seasons (rainy and dry), fecal samples were collected from three to five colonies of M. rufus in the roofs of urban residences. Eight days of sampling were made per season, with a maximum of 15 fecal samples taken per day. To obtain fecal samples, we used the methodology used by Pokhrel & Budha (2014)POKHREL S & BUDHA PB. 2014. Key to identify insects from droppings of some insectivorous bats of Nepal. J Inst Sci Technol 19(1): 129-136., adapted for the roofs of residences. Plastic (smooth and previously cleaned, 1 m × 1 m) was used for 24 h inside the shelter, under the colony, to collect only fresh samples. Before the collection of feces, individuals were captured from each colony for identification and confirmation of the species present at the site. Individuals were identified with the help of the identification keys of Gregorin & Taddei (2002)GREGORIN R & TADDEI VA. 2002. Chave artificial para a identificação de molossídeos brasileiros (Mammalia, Chiroptera). J Neotrop Mammal 9(1): 13-32. and Reis et al. (2017)REIS NR, PERACCHI AL, BATISTA CB, LIMA IP & PEREIRA AD. 2017. História natural dos morcegos brasileiros: chave de identificação de espécies, 1a ed. Rio de Janeiro: Technical Books Editora, 416 p. and later released. Fecal samples of bats were placed in Eppendorf® tubes containing 70% alcohol and stored in a refrigerator until analysis.

All procedures used in this study, referring to the management of animals, followed the guidelines for capture, handling, and care of mammals, according to Sikes and American Society of Mammologists (2016)SIKES RS & AMERICAN SOCIETY OF MAMMALOGISTS. 2016. Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 97(3): 663-688. and with the authorization of the Ethics Committee on the Use of Animals of the University State of Maringá (Process 4182101018).

It is known that there is a difference in the diet between male and female bats, especially among reproductive distinct stages (Wilkinson & Barclay 1997WILKINSON LC & BARCLAY RMR. 1997. Differences in the foraging behaviour of male and female big brown bats (Eptesicus fuscus) during the reproductive period. Écoscience 4(3): 279-285.). In this study, however, the chosen methodology did not favor this type of information collection.

Analyses

The insect identification was made by morphological analysis of the fragments found in bat feces according to Whitaker et al. (2009)WHITAKER JO, MCCRACKEN GF & SIEMERS BM. 2009. Food habits analysis of insectivorous bats. In: KUNZ TH and PARSONS S (Eds), Ecological and behavioural methods for the study of bats, Baltimore: Johns Hopkins University Press Baltimore, USA, p. 567-592., with the determination at the order or family level, using stereomicroscope. Insect identification was restricted to hard parts that can be visually identified. Each fecal sample was examined separately, obtaining the percentage of volume and the frequency of each identified item. The volume of each food item was determined using a gridded dish, thus obtaining the volume in mm³, which was later transformed into mL (Hellawell & Abel 1971HELLAWELL LM & ABEL R. 1971. A rapid volumetric method for the analysis of the food of fishes. J Fish Biol 3(1): 29-37.). Insect fragments that cannot be confidently distinguished were treated as unidentified insects (U. I.).

To characterize the species diet, the Feeding Index (IAi%) was calculated to distinguish the relative importance of each item in the species’ diet (Kawakami & Vazzoler 1980KAWAKAMI E & VAZZOLER G. 1980. Método gráfico e estimativa de índice alimentar aplicado no estudo de alimentação de peixes. Bol Inst Oceanogr São Paulo 29(2): 205-207.), using the following formula:

where IAi = feeding index; i = is each food item; F = occurrence frequency (%); V = volume (%). IAi is an index that varies from 0 to 1.

Seasonal difference in diet species composition, considering the rainy season and dry, was evaluated using a Permutational Multivariate Analysis of Variance, PERMANOVA (Anderson et al. 2008ANDERSON MJ, GORLEY RN & CLARKE KR. 2008. PERMANOVA + for PRIMER: guide to software and statistical methods. Plymouth, UK: PRIMER-E, 214 p.), with a Bray Curtis similarity matrix generated from the data of volume of food items. The analysis was performed using PRIMER software version 6.0 (Anderson et al. 2008ANDERSON MJ, GORLEY RN & CLARKE KR. 2008. PERMANOVA + for PRIMER: guide to software and statistical methods. Plymouth, UK: PRIMER-E, 214 p.).

To determine the relative level of specialization in the bat diet, the standardized trophic niche breadth was calculated using the standardized Levins index (Hurlbert 1978HURLBERT SH. 1978. The measurement of niche overlap and some relatives. Ecology 59(1): 67-77.), which ranges from 0, when the species consumed only one type of food, to 1, when the species consumed several food types.

where Ba = standardized trophic niche breadth; P_ij = is the proportion of the food item in the species’ diet; n = refers to the total of food items.

To relate the food items found in the bats’ diet with the insect families that cause damage to agriculture, three references were used: Chagas et al. (2016)CHAGAS F, POLONIO JC, RUVOLO-TAKASUSUKI MCC, PAMPHILE JÁ & CONTE H. 2016. Controle biológico em sistema orgânico de produção por agricultores da cidade de Maringá (Paraná, Brasil). Ciênc Nat 38(2): 637-647. and Albuquerque et al. (2002)ALBUQUERQUE FA, PATTARO FC, BORGES LM, LIMA RS & ZABINI AV. 2002. Insetos associados à cultura da aceroleira (Malpighia glabra L.) na região de Maringá, Estado do Paraná. Acta sci Biol Sci 24(5): 1245-1249., which addresses groups of insects that damage agriculture in the region of the municipality of Maringá, and, Garcia (2007)GARCIA AH. 2007. Levantamento, identificação e avaliação dos danos de insetos em árvores ornamentais na área urbana de Goiânia (GO). Pesq Agropec Trop 29(1): 77-81., that identify the insects considered pests in an urban environment, as they cause damage to ornamental trees in cities.

RESULTS

In the total of 140 samples collected, 92 were during rainy season, and 48 were in the dry season. Eight insect orders were identified, six of which were present in the rainy season sampling and seven that were present in the dry season. In terms of volume percentage, the M. rufus diet consisted mainly of Hymenoptera (46.9%), for the rainy season, and Coleoptera (39.2%), for the dry season (Table I). The order Coleoptera (73.9% and 95.8%, for the rainy and dry season, respectively) was the food item most frequently consumed in both seasons, followed by the orders Hemiptera (69.6%) in the rainy season and Lepidoptera (77.1%) in the dry season (Table I).

According to the Feeding Index (IAi%), the most relevant items consumed were Hymenoptera (46%), in the rainy season and Coleoptera (49.5%), in the dry season (Table I). The trophic niche breadth did not vary between the seasons, for the rainy season, Ba = 0.36 and for the dry season, Ba = 0.37, which indicates the high specialization of M. rufus, regardless of seasonality. PERMANOVA identified significant differences in the specie diet composition according to the seasons evaluated (F = 3.69; P = 0.023). Considering that Trichoptera was recorded only in the rainy season, in addition to Diptera and Neuroptera that were recorded only in the dry season.

Five families (Hymenoptera: Formicidae; Hemiptera: Pentatomidae and Cicadellidae; Coleoptera: Chrysomelidae and Curculionidae) were identified as insect pests (Figure 2). Regarding the frequency of occurrence of these taxa, Formicidae (47.8%) was the most frequent in the diet during the rainy season and Chrysomelidae (79.2%), which is associated with damage to local agriculture, was the food item most consumed during dry season (Table II).

Figure 2
Food items were found in fecal samples of Molossus rufus, in a tropical urban environment in southern Brazil, from November 2018 to September 2019. a and b - Coleoptera: Chrysomelidae (Diabrotica sp.); c - Coleoptera; d and e - Hemiptera: Cicadellidae; f and g - Hemiptera: Pentatomidae; h and i - Lepidoptera (scale and eggs); j, k and l - Hymenoptera: Formicidae; m - Diptera; n - Isoptera; o and p - Coleoptera: Curculionidae; q - Trichoptera (larva); r - Neuroptera.

DISCUSSION

The composition of the M. rufus diet revealed the most consumed food items during the two seasons, with a reduced number of samples in the dry season. The most consumed orders by M. rufus were Hymenoptera, Coleoptera, and Hemiptera, also evidenced by Marques (1986)MARQUES SA. 1986. Activity cycle, feeding and reproduction of Molossus ater (Chiroptera: Molossidae) in Brazil. Bol Mus Para Emilio Goeldi Ser Zool 2(2): 159-179., who analyzed the diet of the species in a house roof in northern Brazil, and Gnocchi et al. (2019)GNOCCHI AP, HUBER S & SRBEKARAUJO AC. 2019. Diet in a bat assemblage in Atlantic Forest in southeastern Brazil. Trop Ecol 60: 389-404., in a study in the Atlantic Forest of southeastern Brazil.

The high frequency of occurrence observed for Lepidoptera fragments in the samples may be associated with the fact that parts of these insects can remain in the digestive tract of bats and be detected for several days (Whitaker et al. 2009WHITAKER JO, MCCRACKEN GF & SIEMERS BM. 2009. Food habits analysis of insectivorous bats. In: KUNZ TH and PARSONS S (Eds), Ecological and behavioural methods for the study of bats, Baltimore: Johns Hopkins University Press Baltimore, USA, p. 567-592.). Thus, even low consumption could lead to their permanence until complete elimination. Occasional food items can also be observed in the diet of M. rufus, as occurred for Trichoptera, which had only one record. The order is commonly found in the diet of bats, with records for Vespertilionidae (Whitaker 2004WHITAKER JO. 2004. Prey selection in a temperate zone insectivorous bat community. J Mammal 85(3): 460-469.). Intensely fragmented food items were frequent throughout the study, a fact that may be related to the morphology of the snout of M. rufus, which, according to Nolte et al. (2009)NOLTE MJ, HOCKMAN D, CRETEKOS CJ, BEHRINGER RR & RASWEILER IV JJ. 2009. Embryonic staging system for the Black Mastiff bat, Molossus rufus (Molossidae), correlated with structure-function relationships in the adult. Anat Rec 292(2): 155-168., allows the food to be kept longer in the mouth until swallowing, thus being chewed more often.

Considering seasonality, the most important food item for the rainy season was Hymenoptera, and for the dry season, it was Coleoptera. These orders are among those with the highest species richness on the planet (Miličić et al. 2021MILIČIĆ M, POPOV S, BRANCO VV & CARDOSO P. 2021. Insect threats and conservation through the lens of global experts. Conserv Lett 14: e12814.). With this, urban environments, characteristically altered and with lower richness (McIntyre 2000MCINTYRE NE. 2000. Ecology of Urban Arthropods: A Review and a Call to Action. Ann Entomol Soc Am 93(4): 825-835.), tend to favor tolerant species belonging to these groups. Seasonal changes such, as low temperatures, can influence bat activity reducing the foraging activity (Wojciechowski et al. 2007WOJCIECHOWSKI MS, JEFIMOW M & TĘGOWSKA E. 2007. Environmental conditions, rather than season, determine torpor use and temperature selection in large mouse-eared bats (Myotis myotis). Comp Biochem Physiol 147(4): 828-840.). However, the range breadth of M. rufus did not change seasonally. M. rufus contributed to the suppression of insects that can cause damage to plants, including ornamental tree species (Chagas et al. 2016CHAGAS F, POLONIO JC, RUVOLO-TAKASUSUKI MCC, PAMPHILE JÁ & CONTE H. 2016. Controle biológico em sistema orgânico de produção por agricultores da cidade de Maringá (Paraná, Brasil). Ciênc Nat 38(2): 637-647., Garcia 2007GARCIA AH. 2007. Levantamento, identificação e avaliação dos danos de insetos em árvores ornamentais na área urbana de Goiânia (GO). Pesq Agropec Trop 29(1): 77-81., Albuquerque et al. 2002ALBUQUERQUE FA, PATTARO FC, BORGES LM, LIMA RS & ZABINI AV. 2002. Insetos associados à cultura da aceroleira (Malpighia glabra L.) na região de Maringá, Estado do Paraná. Acta sci Biol Sci 24(5): 1245-1249.).

There was a shift in the consumption of Hemiptera by M. rufus, relative to the composition of the families between the two seasons, changing the consumption of Pentatomidae for Cicadellidae. This may be related to the availability of some types of insects in the urban environment, as in the population fluctuation of Cicadellidae in a citrus orchard in the State of São Paulo (Yamamoto et al. 2001YAMAMOTO PT, JUNIOR WDP, ROBERTO SR, FELIPPE MR & FREITAS EP. 2001. Flutuação Populacional de Cigarrinhas (Hemiptera: Cicadellidae) em Pomar Cítrico em Formação. Neotrp Entomol 30(1): 175-177.). Population fluctuations can influence the availability of predators. Insectivorous bats that inhabit places where food availability is limited, their diet remains similar to the abundance of insects available in the environment, that is, a more restricted diet (Whitaker 2004WHITAKER JO. 2004. Prey selection in a temperate zone insectivorous bat community. J Mammal 85(3): 460-469.).

The constant consumption of the two main families found in the diet, Formicidae (in this case, winged ants) and Chrysomelidae, indicates that M. rufus contributes to the control of these arthropods in the environment. The consumption of the family Chrysomelidae was marked by the presence of Diabrotica sp., which can be considered a pest. Diabrotica speciosa, at its larval stage, reduces the efficiency of the root system of corn, reducing the height and the dry weight of the plant, while the adult insect consumes the leaf area, mainly legumes, such as beans and soybeans, but also grasses, such as corn and rice (Marques et al. 1999MARQUES GBC, ÁVILA CJ & PARRA JRP. 1999. Danos causados por larvas e adultos de Diabrotica speciosa (Coleoptera: Chrysomelidae) em milho. Pesqu Agropec Bras 34(11): 1983-1986.). This insect is considered a pest in agriculture for damaging foods of high economic value (Teodoro et al. 2014TEODORO JS, TRECHA CO, MEDINA LB, HELLWIG L, LIMA CV & ROSA APSA. 2014. Biologia e tabela de vida de fertilidade de Diabrotica speciosa (Col.: Chrysomelidae) em dieta natural. Arq Inst Biol 81(3): 238-243.). There is no evidence that insects of this genus can cause major economic impacts in urban centers; however, the family Chrysomelidae is capable of affecting species used in urban afforestation (Garcia 2007GARCIA AH. 2007. Levantamento, identificação e avaliação dos danos de insetos em árvores ornamentais na área urbana de Goiânia (GO). Pesq Agropec Trop 29(1): 77-81.), in addition to small ornamental plants. Thus, this consumption represents an ecosystem service that the bat provides by removing this insect from the environment.

Our results showed that the feeding habit of M. rufus in an urban tropical environment in southern Brazil was composed mainly of Hymenoptera in the rainy season and Coleoptera in the dry season, in addition to having specialized diet, with a narrow trophic niche breadth. This leads us to infer about the important ecosystem service that insectivorous bats provide in urban centers, through feeding and thus reducing the abundance of the population of insects that can cause some damage to society’s resources, as in the reduction of possible vectors of agricultural pests.

ACKNOWLEDGMENTS

The authors would like to thank all members of the Study Group on Mammal Ecology and Environmental Education (GEEMEA) for their support. We thank Zootech for providing capture equipment. To Camila Sant’Anna and Ana Carolina Horta for their help during sampling and analysis. To the Graduate Program in Comparative Biology (PGB) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship, which is essential as an incentive and for the development of Brazilian scientific research.

REFERENCES

Publication Dates

History