Activity of the Insectivorous Bat Pteronotus Parnellii Relative to Insect Resources and Vegetation Structure

Journal of Mammalogy, 96(5):1036–1044, 2015 DOI:10.1093/jmammal/gyv108

Activity of the insectivorous bat Pteronotus parnellii relative to insect resources and vegetation structure

Leonardo Queiroz de Oliveira, Rodrigo Marciente, William E. Magnusson, and Paulo Estefano D. Bobrowiec* Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia (INPA), Av. André Araújo 2936, CP 2223, Manaus-AM 69080-971, Brazil Downloaded from https://academic.oup.com/jmammal/article-abstract/96/5/1036/917312on19May2020 guest by fromDownloaded * Correspondent: [email protected]

Riparian areas oten are assumed to be necessary sites or oraging by insectivorous bats because o high insect availability and ease o movement and echolocation in the orest. However, eects o vegetation clutter and insect availability on bat activity have not been compared between riparian and nonriparian areas. We used autonomous recorders to evaluate the eects o vegetation structure, insect mass, and assemblage composition on the activity o the aerial insectivorous bat Pteronotus parnellii along stream channels and nonriparian areas in a tropical rainorest in central Brazilian Amazonia. We quantied vegetation clutter using horizontal photographs, captured nocturnal insects with light traps, and recorded bat activity or 110 nights (1,320 h) in 22 sampling plots. Pteronotus parnellii was more active in sites with dense understory vegetation, which were more common away rom riparian zones. Bat activity was related to insect availability (mass and composition), independent o the habitat type. Ability to detect insects on vegetation and avoid obstacles should not restrict the activity o P. parnellii in cluttered sites. This suggests that mass and species composition o insects had stronger infuences on habitat use than did vegetation clutter. Pteronotus parnellii probably selects cluttered places as eeding sites due to the availability o higher quality prey.

Áreas ripárias são muitas vezes consideradas locais necessários para o orrageio por morcegos insetívoros por causa da alta disponibilidade de insetos e acilidade de movimento e recepção da ecolocalização na foresta. No entanto, os eeitos da obstrução da vegetação e disponibilidade de insetos sobre a atividade de morcegos não têm sido comparados entre as áreas ripárias e não ripárias. Nós usamos gravadores autônomos de ultrassom para avaliar os eeitos da estrutura da vegetação, massa e composição da assembleia de insetos sobre a atividade do morcego insetívoro aéreo Pteronotus parnellii ao longo do canal central de riachos e áreas não ripárias em uma foresta tropical na Amazônia central brasileira. Nós quanticamos a obstrução da vegetação usando otograas horizontais da foresta, capturamos os insetos noturnos com armadilhas luminosas e gravamos a atividade dos morcegos durante 110 noites (1.320 h) em 22 pontos de amostragem. Pteronotus parnellii oi mais ativo em locais com vegetação arbustiva densa, que oram mais comuns longe das zonas ripárias. A atividade dos morcegos oi relacionada com a disponibilidade de insetos (massa e composição), independente do tipo de habitat. A capacidade de detectar insetos sobre a vegetação e evitar obstáculos não deve restringir a atividade de P. parnellii em locais obstruídos. Isto sugere que a massa e a composição de espécies de insetos tiveram orte infuência sobre o uso do habitat do que a obstrução da vegetação. Pteronotus parnellii provavelmente seleciona lugares obstruídos como locais de alimentação devido à disponibilidade de presas de maior qualidade.

Key words: Central Amazon, Chiroptera, oraging habitat, orest structure, insect availability, Mormoopidae, riparian zone, tropical orest, vegetation clutter © 2015 American Society o Mammalogists, www.mammalogy.org

The distribution o many bat species has been associated with more requently (Fukui et al. 2006; Hagen and Sabo 2011). For ood abundance and vegetation structure (Sleep and Brigham insectivorous species, ood abundance, echolocation, and the 2003; Kusch et al. 2004; Rainho et al. 2010). In general, areas ability to detect prey may be the most necessary determinants that avor movement and have high ood availability are visited o habitat use (Aldridge and Rautenbach 1987). Vegetation 1036 DE OLIVEIRA ET AL.—HABITAT SELECTION IN PTERONOTUS PARNELLII 1037 and other nonprey objects are sources o echoes that interere Pteronotus parnellii is an insectivorous bat that uses high- with bat navigation. The risk o collision and the diculty o duty-cycle echolocation that is well suited to detecting fut- achieving aerial maneuvers reduce fight eciency in cluttered tering targets in cluttered habitats (Lazure and Fenton 2011; areas (Norberg and Rayner 1987; Schnitzler and Kalko 2001). Fenton et al. 2012). The study was undertaken in a 25-km2 Furthermore, dense vegetation may interere with the detection area o continuous orest in central Brazilian Amazonia, where o potential prey (Kusch et al. 2004; Jones and Holderied 2007; we monitored bats by use o automated ultrasound detectors Rainho et al. 2010). Structural complexity o vegetation may located in streamside and nonriparian areas. We hypothesized infuence bat oraging as they may avoid navigating in cluttered that vegetation structure and availability o insect prey aect sites (Sleep and Brigham 2003; Ober and Hayes 2008; Jung the activity o the species and that activity diers between et al. 2012). riparian and nonriparian areas. As clutter levels are high in the Bats may overcome the physical constraints o vegetation understory o the Amazon rainorest, but less in riparian zones, by using trails in the orest (Law and Chidel 2002; Sleep and we expected that P. parnellii would concentrate its activity in https://academic.oup.com/jmammal/article-abstract/96/5/1036/917312on19May2020 guest by fromDownloaded Brigham 2003). Small orest streams and riparian zones re- uncluttered corridors o orest streams and areas with higher quently are used by many insectivorous bat species because insect availability. they create gaps in the orest. Small streams avor the movement o understory bats more than do cluttered nonriparian habitats (Fukui et al. 2006). Small streams oten have low Materials and Methods vegetation density and orm open corridors allowing aster Study site.—The study was conducted in the Reserva Ducke movement o bats by acilitating maneuverability and echo- (2°58′S, 59°55′W; Fig. 1), located to the north o the city o location (Fukui et al. 2006; Hagen and Sabo 2011). Bats can Manaus at Km 26 o the AM-110 Highway, Amazonas State, use a stream channel to commute more easily between sites, Brazil. The reserve is part o the Brazilian Long-term Ecological avoiding more cluttered areas inside the orest (Ober and Research Program o the Brazilian National Research Council Hayes 2008). (Programa de Pesquisas Ecológicas de Longa Duração - PELD/ Forest streams and riparian zones have a signicant infuence CNPq). It covers 10,000 ha o lowland rainorest. Annual rain- on the distribution o insects in the orest and represent a orag- all varies between 1,750 and 2,500 mm, with the highest rain- ing habitat or many species o insectivorous bats (Jong and all between November and May and a drier period between Ahlén 1991; Wickramasinghe et al. 2003; Fukui et al. 2006; June and October (Oliveira et al. 2008). Mean relative humid- Hagen and Sabo 2014). Insect availability along river channels ity was 86%, and mean annual temperature was 26°C (Ribeiro is known to be relatively high compared to nonriparian zones et al. 1999). The relie is undulating with small plateaus, slopes, because the water bodies provide habitat or aquatic insects and valleys that vary between 45 and 140 m in height. Small (Fukui et al. 2006; Hagen and Sabo 2014). Higher concentra- streams are ound in valley bottoms. The orest canopy is tions o insects and ease o travel and prey capture may result in generally 30–35 m though emergent trees may exceed 50 m a higher activity o aerial insectivorous bats above stream chan- (Ribeiro et al. 1999). nels (Sleep and Brigham 2003; Wickramasinghe et al. 2003; The 25 km2 (5 × 5 km) trail system was established accord- Lloyd et al. 2006; Ober and Hayes 2008; Hagen and Sabo 2011, ing to RAPELD methodology (Magnusson et al. 2005, 2014) 2014). that consists o a grid o 6 trails oriented north-south and 6 Several studies have investigated the eect o vegetation trails oriented east-west (Fig. 1). The trails give access to 30 structure, insect availability, and stream corridors in riparian uniormly distributed study plots, each separated rom the next areas on the spatial distribution o aerial insectivorous bats by 1,000 m. Within the grid, there are also 15 riparian plots (Grindal et al. 1999; Wickramasinghe et al. 2003; Fukui et al. located along streams (Fig. 1). The plots were 250 m long. The 2006; Ober and Hayes 2008; Jung et al. 2012). However, the uniormly distributed plots ollowed the topographic contour in relative importance o these 3 actors rarely has been evaluated order to minimize internal heterogeneity in soil properties and simultaneously (Ober and Hayes 2008; Hagen and Sabo 2011). drainage, which oten correlate with plant assemblage structure Most studies have been conducted along a single stream chan- (Magnusson et al. 2005). Riparian plots ollowed the banks o nel, many in areas strongly impacted by humans (Sleep and streams. Brigham 2003; Lloyd et al. 2006; Ober and Hayes 2008; Jung Study species.—Pteronotus parnellii is a medium-sized et al. 2012; Hagen and Sabo 2014). This neglects the possible understory-dwelling Neotropical bat with body length o 7.3– infuence o nonriparian sites in continuous orest or the dis- 10.2 cm, wingspan o 30–35 cm, and body mass o 10–20 g tribution o bats. Furthermore, most studies classiy vegetation (Herd 1983). Its wings are broad, rounded on the tips, and have clutter in qualitative categories (e.g., complex versus simple low wing loading (Emrich et al. 2014). The species uses high- understory; open versus closed vegetation), instead o using duty-cycle echolocation and produces search-phase signals vegetation clutter as a quantitative variable. Herein, we evaluate characterized by a long constant requency (Rydell et al. 2002; how the structural characteristics o vegetation and the avail- Jones and Teeling 2006). Wing characteristics and high-duty- ability o insect prey infuence bat distribution in riparian and cycle echolocation suggest that P. parnellii is well suited or nonriparian zones using Pteronotus parnellii (Mormoopidae) hunting fying insects in cluttered vegetation (Vater et al. 2003; as a model species. Jones and Teeling 2006; Emrich et al. 2014). The species occurs 1038 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/article-abstract/96/5/1036/917312on19May2020 guest by fromDownloaded

Fig. 1.—Location o Reserva Ducke to the north o Manaus, Amazonas State, Brazil. Topography and stream distribution in the RAPELD grid is shown in detail. Open circles represent nonriparian plots and open squares represent riparian plots adjacent to streams.

rom the northern coastal plans o the Gul o Mexico, along the the riparian plots, we used one 3-m-long cable to position the Caribbean coast, to Trinidad and the Amazon basin, and south microphones over the center o the stream. to the northern part o Mato Grosso State, central Brazil (Patton The SM2+ units were programed to create audio les in a and Gardner 2007). The species occurs in a variety o orest WAC ormat at intervals o 30 min, producing as many as 24 types, rom lowland rainorest to drier orest, and at elevations les or each 12-h sampling period. Each WAC le was con- rom sea level to 3,000 m (Smith 1972; Handley 1976). Recent verted to WAV ormat and divided into segments o 5-s duration molecular studies supported by acoustics data have shown that using the program Kaleidoscope (Wildlie Acoustics, Maynard, P. parnellii is composed o several cryptic species that may not Massachusetts). The acoustic signals were visualized with the be related to original P. parnellii native to Jamaica (Clare et al. Avisot-SASLab Pro program, version 4.34 (Specht 2005). 2013; Thoisy et al. 2014). These studies show that the echo- Spectrogram resolution characteristics were set to a hamming location call requency may indicate distinct species. All bats evaluation window with a ast Fourier transormation o 512 recorded in Reserva Ducke emitted calls o 55 kHz, overlap- points and a rame size o 100%. One bat acoustic signal was ping with those o specimens rom French Guiana and Amapá dened as a 5-s segment that contained 2 or more P. parnel- (Brazil). lii search-phase calls. Data were expressed as the number o Bat activity.—We recorded the bat search-phase calls rom search-phase calls per night per recording plot (total number o January to May 2013 during the rainy season. We sampled search-phase calls/5 nights). No eeding buzz was recorded in 22 plots (Fig. 1), 12 in nonriparian and 10 in riparian areas. the segments that were analyzed. The nonriparian plots were separated by 1–6 km, and the Understory-vegetation clutter.—We measured vegetation riparian plots were separated by 0.56–5.2 km. The distance clutter using horizontal photographs o vegetation, adapted between riparian and nonriparian plots varied rom 0.4 to 8.1 rom the method o Marsden et al. (2002). A white cloth was km. Each plot was sampled or 5 consecutive nights between mounted in a 3 × 3 m aluminum rame to create a panel that 1800 and 0600 h (12 h per night), resulting in 60 h o record- contrasted with the vegetation (Supporting Inormation S1). ings per plot. We monitored the bats with Song Meter SM2+ The white panel was positioned perpendicular to the angle o autonomous recording units coupled to an SMX-US omnidi- vision o a digital camera located 8 m rom the panel. In nonri- rectional ultrasonic microphone (Wildlie Acoustics, Maynard, parian plots, the vegetation was photographed every 10 m along Massachusetts). We recorded bat activity in real time with a a 100 m stretch o the central line o the plot located around sampling requency o 384 Hz, a ull-spectrum resolution o the point where vocalizations were recorded (n = 10 vegeta- 16 bits with a 1-s pretrigger and a 0.1-s posttrigger with Dig tion photographs per plot). In riparian plots, photographs were HPF and Dig LPF deactivated and Trigger Level 0 dB. The made o vegetation over the stream with the white panel posi- SM2+ units were placed in the center o each plot. The micro- tioned perpendicular to the central channel at distances o 10 m phones were positioned at a height o approximately 1.5 m. In along a 180 m transect o the stream course (n = 10 vegetation DE OLIVEIRA ET AL.—HABITAT SELECTION IN PTERONOTUS PARNELLII 1039 photographs per plot). In each plot, we positioned the SM2+ to estimate the independent contribution o each explanatory unit at the midpoint o the transect used to quantiy the vegeta- variable in a multiple GLM test (Mac Nally 2002). The eects tion clutter. o insect-order composition and insect size on bat activity Understory-vegetation clutter was quantied by transorm- were examined with GLM tests. The variance explained by the ing the photographs into black-and-white images so that black GLM analysis was calculated as [1 − (residual deviance o the areas represented vegetation and white areas represented open ull model/deviance o the null model)]. When vegetation clut- space. The black areas or each o the 10 images rom each ter and insect mass were used as response variables, we used a plot were summed to quantiy the percentage o area covered Poisson distribution controlled or overdispersion in the GLM by vegetation, equivalent to one large photograph per plot. We analysis (Zuur et al. 2009). A Gaussian error distribution was used the program ImageJ 1.38x (Rasband 2007) to quantiy the used in analyses o insect-order composition (NMDS axis) vegetation clutter. as the ordination axis was not count data. All analyses were Insect prey.—Flying nocturnal insects were collected in light conducted in the R program, version 2.12.1 (R Development https://academic.oup.com/jmammal/article-abstract/96/5/1036/917312on19May2020 guest by fromDownloaded traps, consisting o a 20-cm diameter plastic cone attached to a Core Team 2014). The NMDS ordination was undertaken in 100-ml insect collecting pot with 70% alcohol. A 25-cm diam- the R package “vegan” (Oksanen et al. 2013) and hierarchical eter plate was suspended above the cone to protect against rain. partitioning in the “hier.part” package (Mac Nally and Walsh To attract insects, a fashlight with 10 LED lights was posi- 2004). tioned beneath the plate and pointed toward the cone. Two light traps were installed per plot at a distance o 70 m rom the SM2+ unit. Light traps remained lit or a 48-h period during the Results time that bat calls were recorded. The light traps were unlikely Light traps captured 1,006 insects rom 12 orders (Table 1). to have aected the oraging behavior o bats, and consequently Total insect mass was 4.2 g (Table 1). Mass o the 6 orders the recordings, as it was not possible to see the light o the traps known to be eaten by P. parnellii comprised 86.3% o the rom where the SM2+ unit was placed. All plots received the total mass o insects, and the most abundant orders (Table 1) same treatment. were Coleoptera (64.5%; 2.7 g), Hemiptera (13.4%; 0.6 g), and Trapped insects were identied to order, and only those orders Diptera (4.1%; 0.2 g). The mass o insects eaten by P. parnellii known to be eaten by P. parnellii were included in the analyses in the nonriparian plots was slightly higher than in the riparian because prey preerences and oraging strategies vary among plots (t = −2.14, d.f. = 20, P = 0.048). Insect-order composi- bat species (Fenton 1990). Identication o insect orders used tion diered between riparian and nonriparian plots (t = 2.24, in the analysis ollowed Role and Kurta (2012) and included d.f. = 20, P = 0.043). Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Vegetation clutter varied rom 43% to 63.8% (X ± Odonata, and Orthoptera. Insects were dried with lter paper SD = 54.9 ± 6.0) in nonriparian plots and between 13.6% and to remove excess alcohol and weighed individually on a pre- 42.8% (27.5 ± 12.6) over the stream channels o riparian plots. cision balance (limit o reading 0.0001 g; Ohaus Discovery, The nonriparian plots had about twice as much cluttering veg- Pine Brook, New Jersey) to estimate the total mass o insects etation as the riparian plots (t = −6.29, d.f. = 20, P < 0.001). captured in each plot. We estimated the average insect mass The distribution o insect orders (Fig. 2) indicated structuring per plot by dividing the mass by the number o insects. Higher o insect assemblages as a unction o vegetation clutter and values indicate plots with larger insects. habitat type. The NMDS ordination axis o the insect orders Data analysis.—We compared vegetation clutter and insect explained 61% o the total variation among plots (NMDS mass between riparian and nonriparian plots using a t-test. stress = 0.12). The insect-order composition (Fig. 3), summa- To evaluate the eect o vegetation clutter on the composi- rized by the single NMDS axis, was related to vegetation clutter tion o insect orders known to be eaten by P. parnellii, we (GLM, r2 = 0.22; t = −2.21; P = 0.039) and diered between used a generalized linear model (GLM). Insect composition riparian and nonriparian plots (t = −2.24; d.f. = 20; P = 0.043). was summarized using nonmetric multidimensional scal- We monitored the activity o P. parnellii or 110 nights and ing (NMDS) with the Bray–Curtis index as the dissimilarity successully recorded ultrasound on 99 nights (90% o record- measure (Legendre and Legendre 1998). We used the mass ing nights). In 1,320 h o recordings, we registered 3,648 o each insect order in the P. parnellii diet as a measure o search-phase calls o P. parnellii (165.8 ± 228.1), o which relative abundance to create 1 NMDS ordination axis. Insect- 3,343 calls were in nonriparian plots (278.6 ± 260.8) and 305 order composition among riparian and nonriparian plots was were in riparian plots (30.5 ± 30.8). Pteronotus parnellii was compared using a t-test. recorded in all 22 plots, and activity varied between 3 and 347 Bat activity (number o search-phase calls per night) calls per plot. Bat activity in nonriparian plots was 9.3 times between riparian and nonriparian plots was compared using greater than in riparian plots (t = −3.27, d.f. = 20, P = 0.007). a t-test. To examine the eect o vegetation clutter and insect Activity o P. parnellii (Fig. 4) was positively related to insect mass on the activity o P. parnellii, we used a multiple GLM mass (GLM, t = 4.17, d.f. = 21, P < 0.001) and vegetation clutter test. A Pearson correlation test indicated little collinear- (GLM, t = 2.28, d.f. = 21, P = 0.034). These variables combined ity between the explanatory variables vegetation clutter and accounted or 65% o the variance explained. Independently, insect mass (r = 0.41). Hierarchical partitioning was employed insect mass and vegetation clutter explained 67% and 33% o 1040 JOURNAL OF MAMMALOGY

Table 1.—Number o individual insects, mass (g), and percentage o the mass o the insect orders collected in Reserva Ducke, Central Amazonia, Brazil. Asterisks indicate orders known to be eaten by Pteronotus parnellii ollowing Role and Kurta (2012).

Insect orders Riparian plots (n = 10) Nonriparian plots (n = 12) Total (n = 22) n Mass (g) % n Mass (g) % n Mass (g) % Hymenoptera* 101 0.2 11.9 155 0.4 14 256 0.6 13.4 Coleoptera* 48 0.6 44.4 110 2.1 73.2 158 2.7 64.5 Diptera* 79 0 0.8 74 0.2 5.5 153 0.2 4.1 Hemiptera* 8 0 0.8 23 0.1 2.2 31 0.1 1.7 Lepidoptera* 44 0.1 4 10 0.1 1.7 54 0.1 2.4 Isoptera 48 0.1 4 5 0 0.3 53 0.1 1.4 Blattodea 5 0 0.2 2 0 0.3 7 0 0.3

Ephemeroptera 184 0.2 16.7 1 0 0 185 0.2 5 https://academic.oup.com/jmammal/article-abstract/96/5/1036/917312on19May2020 guest by fromDownloaded Orthoptera* 36 0 0.8 0 0 0 36 0 0.2 Mantodea 2 0 0 0 0.1 2.7 2 0.1 1.9 Plecoptera 8 0 2.4 0 0 0 8 0 0.7 Trichoptera 63 0.2 14.3 0 0 0 63 0.2 4.3 Total 626 1.3 100 380 2.9 100 1,006 4.2 100

Fig. 2.—Distribution o insect orders along the gradient o vegetation clutter in study plots at Reserva Ducke, Central Amazonia, Brazil. Asterisks indicate the orders o insects eaten by Pteronotus parnellii. Solid bars represent the mass o each insect order in sampling plots. The total or each order is 100%, so it is not possible to make graphical comparisons o total mass between orders, but these are given in Table 1. DE OLIVEIRA ET AL.—HABITAT SELECTION IN PTERONOTUS PARNELLII 1041 Downloaded from https://academic.oup.com/jmammal/article-abstract/96/5/1036/917312on19May2020 guest by fromDownloaded

Fig. 3.—Relationship between the insect-order composition, summarized by a single NMDS axis, and vegetation clutter. Black circles represent nonriparian plots and open circles represent riparian plots. NMDS = nonmetric multidimensional scaling. the response-variable variance, respectively. The activity o P. parnellii was positively associated with mean insect size (GLM, r2 = 0.30; t = 3.13; P < 0.005) and insect-order composition (GLM, r2 = 0.62; t = 5.35; P < 0.001).

Discussion Vegetation clutter was greater in nonriparian than in riparian areas as has been recorded in other regions (Fukui et al. 2006; Hagen and Sabo 2011). Bats tend to be more active along river channels in many areas because the channels acilitate bat movement in orests (Ober and Hayes 2008). However, con- trary to our expectations, the activity o P. parnellii was greater in plots with high levels o vegetation clutter in nonriparian areas. Pteronotus parnellii activity also was higher in plots Fig. 4.—Partial regression results o Pteronotus parnellii activity with a higher mass o insects, regardless o whether the plot (search-phase calls per night) with a) mass o insects known to be part was in riparian or nonriparian areas. Insect mass was greater in o the P. parnellii diet and b) vegetation clutter. Black circles represent more cluttered plots, and this could explain the greater levels nonriparian plots and open circles represent riparian plots. o activity by P. parnellii in areas with more closed vegetation. Although we did not record any eeding buzz, the posi- 2009). The ability to use dierent habitats by bats is related tive association between bat activity and insect availability is to fight and echolocation characteristics. Pteronotus parnellii evidence that the relationship between bat activity and orag- produce long-duration constant requency (CF) signals termi- ing is strong and direct. Plots with highest P. parnellii activity nating with a broadband sweep, which enhance prey localiza- likely are to be the plots with highest oraging activity, indicat- tion (Schnitzler et al. 2003). Long CF signals oten are used by ing higher oraging eort in plots with higher general activity. bats searching or moving targets (prey or vegetation obstacles) These results suggest that insect mass was a greater infuence in cluttered habitats and are associated with Doppler-shit com- on habitat use by P. parnellii than vegetation clutter. pensation (Jones 2005). The wing morphology o P. parnellii is Higher P. parnellii activity in areas with denser vegetation is that o a generalist, with a fexible and adaptable fight, so that not in line with the results o most studies o activity patterns o it may exploit dierent habitats (Marinello and Bernard 2014), aerial insectivorous bats, which reported greater activity above including highly cluttered sites. Ability to detect vegetation streams (Grindal et al. 1999; Fukui et al. 2006; Akasaka et al. objects should not limit P. parnellii fight in orest understory, 1042 JOURNAL OF MAMMALOGY so it can use both riparian and nonriparian areas. This suggests et al. 2002). This can hinder the understanding o the biotic and that the amount o vegetation clutter encountered in this study abiotic actors that infuence habitat selection by bats as the bats did not restrict the activity o P. parnellii. This species probably do not have alternative areas in which to orage. Pteronotus selects cluttered places as eeding sites because it is attracted parnellii is a orest specialist that avoids highly degraded areas by higher quality prey. (Bernard and Fenton 2007; Bobrowiec and Gribel 2010) and The dierence in use o riparian and nonriparian areas should seems to choose closed vegetation to naturally open environ- be more closely correlated with amount and type o insects. Mass ments. In degraded landscapes, this bat may use riparian areas o insects o orders eaten by P. parnellii was higher in nonripar- merely as a reuge. More studies need to be conducted in rela- ian plots and species composition varied between riparian and tively undisturbed areas, with simultaneous monitoring o bat nonriparian areas. The combined mass o Hemiptera, Diptera, activity in riparian and nonriparian areas, to make generaliza- Coleoptera, and Hymenoptera was higher in nonriparian areas. tions about the need or riparian zones by insectivorous bats. These terrestrial insect orders are requent components o the https://academic.oup.com/jmammal/article-abstract/96/5/1036/917312on19May2020 guest by fromDownloaded P. parnellii diet (Emrich et al. 2014). In contrast, aerial aquatic insects (Ephemeroptera, Plecoptera, and Trichoptera), which Acknowledgments are rarely eaten by the species, made up one-third o the insect The study was unded by the Coordenação de Apereiçoamento mass in the riparian plots but were not captured in nonriparian de Pessoal de Nível Superior (CAPES), Centro de Estudos plots. The activity o P. parnellii was strongly aected by insect Integrados da Biodiversidade Amazônica (INCT-CENBAM), composition along a clutter gradient, with activity concentrated and Fundação Amazônica de Deesa da Biosera (FDB). It was in locations with more insects that orm part o its diet. Areas carried out under license rom the Instituto Brasileiro do Meio away rom streams may be necessary because they provided Ambiente e dos Recursos Naturais Renováveis (36748-1). ood resources that are scarce near streams. Field inrastructure was provided by the Programa de Pesquisa Despite the greater availability o ood in nonriparian plots, em Biodiversidade (PPBio) and the Programa de Pesquisa P. parnellii also used riparian areas, although with less inten- Ecológica de Longa Duração (PELD). LQO and PEDB were sity. Riparian areas oten are considered to be important orag- supported by a CAPES scholarship and RM by an INCT- ing areas or insectivorous bats because o the availability o CENBAM scholarship. WEM received a productivity grant aerial aquatic insects (Hagen and Sabo 2014). However, P. par- rom CNPq. We thank R. dos Santos Paz or eld assistance nellii rarely eats aquatic insects (Emrich et al. 2014). Hagen and Á. López Baucells and F. Baccaro or technical suggestions and Sabo (2011) showed that insect resources were more abun- during the study. A. Barnett helped with the English revision. dant in parts o streams where vegetation density was greater, suggesting that sites with highly cluttered vegetation close to a stream channel may provide more terrestrial insects. In our Supporting Information study area, the streams were narrow (< 3.3 m o width) and may The Supporting Inormation documents are linked to this have attracted terrestrial insects rom nearby riparian areas. manuscript and are available at Journal o Mammalogy online Terrestrial insects common in the diet o P. parnellii were cap- (jmammal.oxordjournals.org). The materials consist o data tured in all riparian plots, although their mass averaged lower provided by the author that are published to benet the reader. there than in nonriparian plots. The posted materials are not copyedited. The contents o all Use o cluttered sites demands greater energy expenditure supporting data are the sole responsibility o the authors. to maneuver and avoid obstacles in the understory (Norberg Questions or messages regarding errors should be addressed and Rayner 1987; Schnitzler and Kalko 2001). Flying in more to the author. cluttered sites could be advantageous when they contain more Supporting Information S1.—Method used to quantiy veg- high-quality ood. The extra energy expenditure due to the use etation clutter using digital photographs in nonriparian and o more cluttered plots by P. parnellii may have been compen- riparian plots. sated or by choosing sites containing more large prey. Energy gained per individual prey is higher or large insects (Akasaka et al. 2009). These ndings suggest that oraging activities o Literature Cited P. parnellii in nonriparian zones may be attributable to both Akasaka, T., D. Nakano, and F. Nakamura. 2009. Infuence o quantity and quality o insect prey. prey variables, ood supply, and river restoration on the oraging Many studies o aerial insectivorous bats have been con- activity o Daubenton’s bat (Myotis daubentonii) in the Shibetsu ducted in areas subjected to strong human impacts. These stud- River, a large lowland river in Japan. Biological Conservation 142:1302–1310. ies have ound higher levels o bat activity in riparian zones Aldridge, H. D. J. N., and I. L. Rautenbach. 1987. Morphology, (e.g., Law and Chidel 2002; Fukui et al. 2006; Dodd et al. 2008; echolocation and resource partitioning in insectivorous bats. Stahlschmidt et al. 2012). However, ew studies o bat activity in Journal o Animal Ecology 56:763–778. riparian zones have included closed adjacent undisturbed orest Bernard, E., and M. B. Fenton. 2007. Bats in a ragmented land- (Grindal et al. 1999; Hagen and Sabo 2011). Riparian orests in scape: species composition, diversity and habitat interactions a landscape subject to human modication could be unctioning in savannas o Santarém, Central Amazonia, Brazil. Biological as reuges in an otherwise highly degraded habitat (Robinson Conservation 134:332–343. DE OLIVEIRA ET AL.—HABITAT SELECTION IN PTERONOTUS PARNELLII 1043

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