Bird s and bat s seed disp ersal 1 Diet of Frugivorous Birds and Bats in Monteverde: Potential Seed Dispersal in Naturally Disrupted Areas Yibing Yu Department of Molecular Environmental Biology University of California, Berkeley EAP Tropical Biology and Conservatin Program, Fall 2017 15 D ecember , 2017 ABSTRACT After a natural disruption clear s away the previous plant community, plants from the new vegetation succession will exploit the newly opened up spaces and start growi ng in this area. Seed dispersal by aerial animals is important in the new vegetation succession because it allow s seeds from places relatively far away to access the area. In early October the storm Nate caused flash floods and landslildes, which disturbed many natural habitats in Monteverde . In this study I investiga te d plant species that naturally grow in disrupted areas by looking at what kind of seeds are dispersed by the frugivorous bird s and bat s in Monteverde , and what seeds actually land in an area opened up by the storm recently. I collected fecal samples from birds and bats, and also set seed traps in a newly opened area caused by a flash flood. By analyzing the samples, I found nine species of bird dispersers and two species of bat dispersers, dispersing 19 species seeds from 12 plant families. Throughout my samples I found that both birds and bats ca n contribute to the diversity in a new vegetation succession. Large amount of seeds in the family Passiflo raceae, Piperaceae, Solanaceae and Primulaceae are distributed by birds and bats. O ne species in particula r, Myrsine coriacea , are dispers ed by a varied of birds, and were found in the seed traps too. Therefore Myrsine coriacea in the family Primulaceae , has a high potential of growing in new vegetation succession after this major natural disruption. Dieta de aves y murciÂŽlagos frugÂ’voros en Monteverde: potencial dispersiÂ—n de semillas en Â‡reas naturalmente alteradas. RESUMEN Los ecosistemas naturales estÂ‡n sujetos a alteraciones naturales ocasionadas por factores ambientales como tormentas o huracanes. Est os fenÂ—menos pueden provocar deslizamientos o cabezas de agua que barren con la vegetaciÂ—n de un Â‡rea. Estas Â‡reas recientemente abiertas pueden ser explotadas por nuevas especies, iniciando asÂ’ un proceso de regeneraciÂ—n natural del bosque. La dispersiÂ—n de semillas por animales voladores como aves y murciÂŽlagos puede ser un factor importante en este proceso debido a que permite que semillas de sitios alejados alcancen el Â‡rea recientemente alterada. A principios de octubre del 2017 la tormenta tropical N ate ocasionÂ— cabezas de agua y deslizamientos extensos, provocando grandes alteraciones naturales en el bosque nuboso de Monteverde. Mi objetivo en este estudio fue determinar el potencial de diferentes especies de plantas para llegar a estos sitios altera dos, basado en la dispersiÂ—n de semillas por aves y murciÂŽlagos. ColectÂŽ muestras de heces de aves y murciÂŽlagos las cuÂ‡les
B irds and bats seed dispersal 2 examinÂŽ buscando encontrar semillas. AdemÂ‡s coloquÂŽ trampas de semillas en un Â‡rea naturalmente alterada como consecuencia de una ca beza de agua, la cual se ubicaba a menos de un kilÂ—metro del sitio de captura. Nueve especies de aves y dos especies de murciÂŽlagos presentaron semillas en sus heces. EncontrÂŽ 19 especies de semillas provenientes de 12 familias de plantas. Las familias con mayor cantidad de semillas dispersadas por aves y murciÂŽlagos fueron Passifloraceae, Piperaceae, Solanaceae y Primulaceae. Un especie en particular, Myrsine coriacea, es dispersada fue encontrada tanto en muestras de varias especies de aves como en las tr ampas de semilla. Esto sugiere que algunas de las semillas que alcanzan las Â‡reas alteradas llegan allÂ’ por medio de dispersiÂ—n por animales voladores, promoviendo asÂ’ la regeneraciÂ—n natural en estos sitios. INTRODUCTION Natural disrupti ons, like storms, landslides and flash floods can often clear most of the vegetation out of a natural area. Though it is detrimental to the old community of plant s and animals, it provides opportunities for new plants to colonize these areas. This is becau se resources old vegetation previously occupied such as water, nutrients, and space are now available for seedlings. Years after, the new plant succession will potentialy recover to the degree that the composition of the plant community resembles the nearb y forests (Walker et al . 1996) . Many factors can influence which plant will start growing first in the new vegetation succession. For example, on a landslide the soil compo sition and the chemical properties change dramatically along the gradient of a land slide (Guariguata 1990), so some portion of the landslide might be mor e suitable for plant growth than other parts of the landslide . Favorable environments also vary among different plants. Pioneer species, plants that require more sunlight and less humidi ty, would outcompete the number of plants that cannot tolerate sunlight in a new vegetation succession (Walker et al . 1996). Seed dispersal is also an important factor, because plants can only grow in places where their seeds get dispersed to. Seeds can e ither come from plants on the edges of disturbed areas , or from dee per into the surrounding forest and even other forest patches, depending on the methods the seeds use to get dispersed. There are multiple ways that the seeds can be carried to the target a reas: they can be dispersed by wind , birds, bats and larger mammals. Amon g these methods, seed dispersal by aerial animals can largely influence the composition of the new vegetation succession, because flying animals can travel a long distance they deposi te the seeds . This allows plant species from far away communities to reach newly disturbed areas. According to Lawton and Putz (1988) , in a landslide area, bird dispersal led to the growth plants that are not normally found in the new vegetation succession after a natural disruption. Thus it is important to take seed dispersal by birds and bats into consideration when studying a vegetation succession. The seed dispersal by a e ri a l animals is also closely related to time of the year. In the tropics different plants fruit in different times of the year. Because many birds are migratory, the composition of the bird community also varies throughout the year . Thus time is also a factor people must consider when looking at aerial animal seed dispersal.
Bird s and bat s seed disp ersal 3 The tropical storm Nate , that occurred October 4 11 2017, caused significant disruptions to many C entral American countries including Panama, Costa Rica, Nicaragua , and Honduras (EFE, 2017). In Monteverde, Costa Rica, the amount of rainfall in September 2017 was 518m m, which was 58% higher than the average amount of rainfall in Monteverde in September, which is 328mm (AccuWeather, 2017). The unusual amount of rainfall caused numerous natural disruption, like flash floods, tree falls and landslides. These disruptions w iped out many previous forests and bushes and created new open spaces. These newly opened up areas offer chances for new vegetation succession. Because t here is a diverse bi rd community and bat community i n the cloud forests of Monteverde , these frugivorou s can play the important role of seed dispersers that carry the seeds to these newly opened up spaces (Wenny 1998, Dinerstein 1986) . The seeds that get dispersed in these newly disturbed areas by aerial animals are potential candidates in the new vegetatio n succession. Since there are many new disturbed areas in Monteverde after storm Nate , it provides a good opportunity to study the potential candidates of plant species that can form the new vegetation succession in t hese disrupted areas. Therefore in my p roject, I was interested in find ing out what some of the bird and bat seed dispersers present in Mont everde present in late November are. What seed species can these seed dispersers help disperse? Finally , what pla nt species have higher potential to grow i n a new vegetation succession after the natural disruption ? MATERIALS AND METHODS The methods of this project consist ed of two parts. The first part was to set up seed traps in a flash flood site caused by Nate in Monteverde and look for the seeds that get dispersed to this area. The second part was to set up mist nets near the flash flood site to capture birds and bats and then collect their fecal samples and then identif y the seeds in the samples. Bird Capture The MoSI program created by Institute f or Bird Population is a program that monitors the survivership and migration pattern of migratory bird species in the New World ( Albert et al . 2016 ) The Monteverde Institute , as one of the station in the MoSI program, set up thirteen mist nets in the fore sts of Rachel and Dwight Crandell Memorial Reserve in the late November every year. This year, the mist netting team mist netted birds from November 20th to November 25th. The project opened the mist nets for ten hours per day, from 6:00am to 16:00pm. I at tended the mist netting event with the Monteverde mist netting team everyday. Du ring the mist netting period, I identified and recorded the species of every bird that got caught up in the mist net.using a bird guide ( Henderson & Adams 2010 ). Bat Capture I set up three to four mist nets for ten of the th irteen days from November 20th to December 2 nd to capture bats . I opened the mist nets for two and a half hours per day, from 5:30pm to 8:00pm. The mist netting events happened in five different places: Baj o de Tigre, Instituto de Monteverde, St. Luis, Racheal and Dwight Crandell Memorial Reserve, and Estacion
B irds and bats seed dispersal 4 de Biologica. Similarly I identified and reco rded the species of every bat caught in the mist net using a mammal guide (Reid 1997). Seed Traps I se t up ten seed traps in a flash flood site in the Racheal and Dwight Crandell Memorial Reserve on November 20th and retrieved the traps on December 2nd. Because of the heavy rainfall in the September and during the past storm, the stream across the reserve flushed away the vegetation along its banks and created a open area near the stream. Each trap was a 50 cm*50 cm sized mesh, and was fixed on the ground using four metal pins. Seed Collection During mist netting, I collected bird and bat fecal samples f rom the cloth bags we used to keep the animals , or on the ground if the bird or bat dropped any in the mist nets or when we were processing the animal. I kept each sample in a snap capped tubes using a wooden scoop and tweezers. For each bird fecal sample, I recorded the number of the tube, the date, and the bird species. For each bat fecal sample, I recorded the number of the tube, the date, the location of the mist nets, and the bat specie s. From the seed traps, I collected the seeds or anything tjat look ed like a seed , and recorded the relative loc ation of the trap. I dissected each fecal sample in a petri dish using 70% ethanol under a dissecting scope . If there were seeds in the sample, I then separated the seeds by their morphospecies and kept them i n separate petri dishes. For e ach sample from the seed traps, I examined the sample under a dissecting scope and then separated the seeds. All of the seeds were later identified with the help of Mr. Rodrigo Solano. R ESULTS Composition of captured birds In total I recorded 96 bird captures in the mist nets . There were four recaptured birds. These 92 individuals include d eight families and 30 different species. Among these 30 species, five species were migratory and 25 species were residents . Insectivor e birds made up the largest portion of a ll the birds captured, which had 51 individuals in 18 species and made up 55.21% of all individuals . Nectarivore birds had seven indiv iduals in three species and accounted for 7.29% of all the birds. Because I found arthropod remains even in the frugivorous species, I grouped frugivores an d omnivores into a compound group. T he group had 38 individuals in nine species and account ed for 37.5 % of all of the birds. There were two omnivorous species that were migratory and there were seven species of omnivorous birds thar were resident species (Appendix I) . Composition of captured bats Among the 14 bats we captured, there were 8 species from two families, Phyllostomidae and Vespertilionidae . Except the insectivorous Myo tis keaysi is in the family Vespertilio nidae,
Bird s and bat s seed disp ersal 5 nine species and 13 bats were f rom the family Phyllostomidae. six species of eleven bats account ed for 78.57% of all captures. one species of one nectarivore bat and one species of insectivorous bat each accoun ted for 7.14% of all captures (Appendix II) . Seeds dispersed by birds I found pieces of arthropods in almost all 73 fecal samples I collected from captured birds, while only 15 of the samples containe d seeds in them. These seeds belonged to 10 plant fami lies and 14 species ( Table 1). T he complementary graph of bird species and the accumulate seed species showed a general trend that as the bird diversity increase s , so does the seed richness (Figure 1). A similar patter was found in the correlation between the bird species richness and the diversity of plant families found in the fecal samples (Figure 2). There were in total 85 seeds found in the samples. A black faced solitaire individual carried seeds from the largest number of species . F our spec ies of see ds from 3 families were found in one black faced solitaire sample . O ne sample from an olive striped flycatcher had the most number of seeds: 16 seeds from a Passiflora species in the family Passifloraceae. This was also the most abundant species with 24 in dividuals and had the highest number of seeds, which account ed for 28.24% of all of the seeds. This Passiflora seeds were only found in olive striped flycatcher fecal samples , and 80% of the samples from olive striped flycatcher carried seeds of this speci es . O live striped flycatchers also carried 308 immature seeds from an unidentified plants in the Ericaceae family. Because immature seeds are not able to germinate after the birds dropped them, I didn't include these seeds in the analysis. Nevertheless, th e large number of Ericaceae seeds found in the olive stripe flycatcher suggested that the bird is potentially an important disp erser of this Ericaceae plant. Comparing to the Passiflora sp., Myrsine coriacea from the Primulaceae family is more a generalist in the aspect of its seed dispersers. The plant has the second largest number of individuals , next to the Passiflora sp., but the Myrsine coriacea seeds were found in the samples of two thirds of all the bird disperser species. Table 1 : Bird species that had seeds in their fecal samples, family of the seed species found in the samples, species of these seeds , total number of seeds found in the samples, and the number of samples. Bird Species Plant Family Plant Species # seeds # samples Black faced Solita ire Araliaceae Oreopanax sp. 1 1 Primulaceae Myrsine coriacea 2 1 Rubiaceae Psychotria sp . 7 1 Morphospecies 1 2 1 Black headed Nightingale Thrush Malvaceae Hampea sp. 1 1 Primulaceae Myrsine coriacea 1 1 Blue crowned Motmot Caprifloiaceae Vibur num costaricanum 1 1 Common Chlorospingus Ericaceae Morphospecies 2 2 1 Unidentified Morphospecies 1 5 1 Olive striped Flycatcher Passifloraceae Passiflora sp. 24 4
B irds and bats seed dispersal 6 Primulaceae Myrsine coriacea 4 1 Smilacaceae Smilax sp. 1 1 Orange billed Nighting ale Thrush Ericaceae Morphospecies 1 1 1 Primulaceae Myrsine coriacea 2 1 Plain Wren Gesneraceae Morphospecies 1 6 1 Swaison's Thrush Piperaceae Piper sp.1 5 1 Primulaceae Myrsine coriacea 4 1 Wood Thrush Primulaceae Myrsine coriacea 13 2 Piperace ae Piper sp.2 3 1 Figure 1 : Accumulation curve of seed species number in relation to the number of birds species sampled.
Bird s and bat s seed disp ersal 7 Figure 2 : Accumulation curve of seed families number in relation to the number of birds species sampled. Comparing the Seed Dis persal by Migrant and Resident Birds The number of residents I caught in the mist nets was four times more than the number of migrants I caught, so there were a greater amount of seeds found in the resident fecal samples than those in the migrant fecal sa mples. However, the average num ber of seeds found per sample was not significantly different between residents and migrants (p=0.26; Table 2) . The number of seed species residents carried was also greater than the number of seed species migrant s carr ied , b ut the values of average number of species found in each migrant and resident were also not significantly different from each other (p=0.77). However, in the three species carried by migrants , only one species, Myrsine coriacea , was also carried by residen t species . No seeds from the Piperaceae family were found in the resident sample s , while the m igrants had two piper species. Based on the samples I collected, migrant species and resident species were contributing differently to the seed diversity they dis persed. Table 2 : Number of fecal samples, total number of seeds, total number of seed species, average number of seeds found per sample, average number of seed species found per sample, and average number of seed species found per bird species in residen t birds and migratory birds. n # seeds # species avg.seed/indv. avg.spp/indv. avg.spp/spp. Resident 12 60 12 8.33 1.50 1.71 Migrant 3 25 3 5.00 1.67 1.50 Seeds dispersed by bats I collected seven samples from four species of bats, and five samples fro m two species of bats: Carollia perspicillata and Sturnira ludovici , seven samples contained 662 seeds in total (Table 3) . These seeds are from three families (Piperaceae, Solanaceae and Melastomataceae)
B irds and bats seed dispersal 8 and five species. One of the two species in genus Pi per (Piperaceae) dispersed by Carollia perspicillata ha d 527 individuals and made up 80% of all the seeds. Similar to the olive striped flycatcher, one of the Carollia perspicillata bat carried more than 400 immature Piper sp.1 seeds, together with the 430 seeds from the same plant species, which means that the bat was able to carry a l most double the amount of seeds recorded. Another species of bat, Sturnira ludovici, also carried 42 seeds from another Piper species. S. ludovici was also a common disperser of the plants form the genus Witheringia (Solanaceae), because these bats carried in total 88 seeds from the two Witheringia species . Table 3 : Bat species that had fecal samples that contained seeds, seed family, seed species, total number of seeds, and the number of samples . Bat Species Plant Family Plant Species # seeds # samples Carollia perspicillata Piperaceae Piper sp.1 527 2 Sturnira ludovici Piperaceae Piper sp.2 42 1 Melastomataceae Conostegia sp. 5 1 Solanaceae Witheringia sp.1 26 1 Sola naceae Witheringia sp.2 62 1 Comparing Seed Dispersal by Birds and Bats There was no overlap between the seed species I found in bird samples and bat samples, and in 12 total plant families found, only one family, Piperaceae, was found in both bird and b at samples (Table 4). The samples from the birds that contained seeds were about twice the number of samples bats that had seeds in their fecal matter . However, the number of seeds carried by each bat was significantly higher than the number of seeds carri ed by each bird (p=0.0063). T he average number of species carried by bird s and bat s was not significantly different from each other (p=0.41) (Table 5) . Table 4 : Seed family, seed species, number of the seeds found in bird fecal samples, and the number of the seeds found in bat fecal samples. Plant Family Plant species # seeds in birds # seed in bats Araliaceae Oreopanax sp. 1 Caprifloiaceae Vib u r num costaricanum 1 Ericaceae Morphospecies 1 1 Morphospecies 2 2 Gesneraceae Morphospecies1 6 M alvaceae Hampea sp . 1 Melastomataceae Conostegia sp. 5 Passifloraceae Passiflora sp. 24
Bird s and bat s seed disp ersal 9 Piperaceae Piper sp.1 5 Piper sp.2 3 Piper sp.3 42 Piper sp.4 527 Primulaceae Myrsine coriacea 22 Rubiaceae Psychotria sp. 7 Morphospecie s 1 2 Smilacaceae Smilax sp. 1 Solanaceae Witheringia sp.1 26 Witheringia sp.2 62 Unidentified Morphospecies 1 5 Total 19 spp. 81 662 Table 5 : Number of fecal samples, total number of seeds, total number of seed species, average number of seeds found per sample, average number of seed species found per sample, and average number of seed species found per animal species in birds and bats. n # seeds # species avg.seed avg.spp avg.spp/spp. Bird 15 85 14 5.67 1.53 1.56 Bat 5 662 5 132.40 1.2 0 2.50 Seeds found in the Seed Traps From all of the ten seed traps, 6 species of seeds were found. And among these 6 species, only one species, which was the Myrsine coriacea, overlapped with the seed species found in the bird fecal samples. No seed spe cies found in the seed traps were found in the bat fecal samples. Table 6 : Seed family, Seed species, and the number of seeds found in the seed traps Plant Family Plant species n Asteraceae Morphospecies 1 1 Cecropia Morphospecies 1 1 Moraceae F icus tu erckheimii 2 Melastomataceae Blakea sp. 1 Primulaceae Myrsine coriacea 13 Unidentified Morphospecies 1 1
B irds and bats seed dispersal 10 DISCUSSION Bird and Bat Dispersers I found nine species of bird dispersers dispersing 14 species of seeds from ten different families . Despit e the fact tha t I only collected a relatively small number of samples in a short period , these indicate a positive correlation between the seed species and family diversity and the bird richness (Fi gures 1, 2). Though o n average each bird species did not d isperse many species of seeds: usually no more than two, the seed species carried by different types of bird s rarely overlap ped with eac h other (Table 1). Other studies also reported this increase in seed dispersal with increasing animal richness. A study on seed dispersal by Turdidae species found that seed ab undance, seed richness and the number of seeds l anding in open areas have a positive correlation with the amount of bird species present (Rodriguez et al . 2017). The study also showed that as the numb er of bird species decrease s , both t he seed abundance and the number of seeds landing in the open area decrease linearly, while the seed richness decreases sigmoidally, indicating the importance of bird richness to seed diversity (Rodriguez et al . 2017). S uch a pattern was also found in other taxonomic groups of animals (Gra cÂ’a and MartÂ’nez 2013, Schleuning et al . 2015) . A noticable group of bird dispersers is the Turdidae family , usually known as the thrushes. A bout half of the bird disperser species I fo und in the study was from the family Turdidae, and nearly half of the total number of bird samples were from thrushes. Both of the two migratory bird seed dispersers: the wood thrush and the swaison 's thrush , are turdids. The study done by Rodriguez and co llaborators ( 2017 ) found that some thrush species could deposit more seeds in to the open areas than others because they more regularly perch in open places. Therefore it will be interesting to investigate more about the behavior of the thrush species in Mo nteverde and find out whether some of these species can have a larger influence in the number of seeds brought over to the open areas by birds. Though it is true that thrush es are an important group of frugivorous birds, it might be overrepresented in the group of dispersers I found in my result. Since the mist nets were placed at ground levels, I was only able to catch and study dw ellers in the forest understory, which happens to be the case for most Turdidae species. Many non understory bird species can a lso serve as important seed dispersers . According to Wenny's study in 1993 and 1998, birds that live in the upper forest story, like resplendent quetzals, bellbirds , and toucanets also contrib ute a lot to the seed dispersal in a neotropical forest. They ar e the important dispersers of the Lauracea e plants (Wenny 1998) , a plant family not represented in my seed collection. Besides, I was only able to catch birds with relatively sm all body sizes in the mist nets, and what seeds the bird can consume largely de pend on their body sizes. The onl y seed species from the Caprifol iaceae family, Viburnum costaricanum , was found in the fecal sample of a blue crowned motmot (Table 1) . The seed was larger than most of the other seeds, and the blue crowned motmot was the l argest seed disperser I captured in the mist net. Bl ack guan is another large size bird dispersers long known for their diverse diet and strong seed dispersal ability (Wenny 1993). I n the study by a former EAP student on the seed dispersal by black guans, he found seven species of seeds in the droppings of the black guans. Surprisingly, in these seven species, only two species of seeds overlap p ed with the seeds species I found in my samples (Coleman 2015). And one of the two overlapping species is Viburnum costaricanum , the species car ried by the blue crowned motmot. The other overlapping species is Myrsine coriacea , the most co mmon seed found in the samples.
Bird s and bat s seed disp ersal 11 Migrant versus Resident species Among the 14 species of seed found in bird samples, resident speci es were found to disperse 12 species of seeds, and migratory species were found to disperse three species of seeds (Table 2). Notic e ably, among the three species of seed s found in migrant fecal samples, the two Piper species were unique to the migratory sp ecies samples. Interestingly, when the study of Rodriguez and collaborators ( 2017) compared the effect of the removal of randomly selected thrush species the migratory thrush species, the disappearance of the migratory species had stronger negative correla tions with the seed richness, seed abundance and the number of seeds dropped in the open microhabitats . Even though the research ers studied the thrushes in a temperate zone, it supported the importance of the migratory species in the ecological service of seed dispersal. Bat Dispersers and Comparing Birds and Bats I found t wo species of bats dispers ing five species of seeds from three plant families (Table 3) . None of the se ed species found in the bat samples were found in the bird samples, and only the P iperaceae family were found in both bird and bat samples. In another bat mist netting study, in total 18 seed species in 11 families were found in the samples from nine frugivorous bats ( Aguilar Garavito et al . 2014). In my research , besides the six captur es of Carollia perspicillata and Sturnira l udovici from which I collected samples, I also captured five individuals of four other frugivorous bat species (Appendix II). One difference between bird and bat dispersers is that a ccording to the samples I coll ected, the bat community had a larger pe rcentage of frugivores than the bird community . The actual proportion of the frugivorous bats can be very different from the estimation made from the captured bats records due to the small bat sample size. However, a past bat mist netting study showed that frugivore bats a c counted for as much as more than 95% of all captures, supporting the relativ ely greater ratio between fruit eating bats and bats having other diets ( Aguilar Garavito et al . 2014) . Another differenc e between bird and bat dispersers is that each frugivore bat carried many more seeds than each frugivore bird . Similar patterns were found in other researches about the birds and bats seed dispersal (Medellin & Osiris 1999, Thomas 1991). A possible reason is that frugivorous bats are more obligate d to a fruit diet than birds. O nly plant matters were found in frugivore bat fecal samples, while arthropod remains were found in almo st all of the frugivorous bird samples . Plants that rely on seed dispersal by ba ts can develop a strong mutualistic relationship with the bats. For example, some Piper species produces poor nutrition fruit so that the bat needs to consume a large amount of fruit to meet its nutrition needs (Fleming, 1986). In this way, a single bat ca n defecate thousands of seeds in one night. The plants also depend on the bats to remove the pulp from the seeds and thus increase the seed germination performance (de Carvalho Ricardo et al . 2013, Robertson et al . 2006 ). Howeve r, having more seeds in a si ngle defecation does not mean a high rate of germination . A cluster of too many seeds will increase the competition between each seeds for limited resources, like the nutrition and spaces for growth. Thus, we are not able to conclude that compared to a fru givorous bird, a frugivorous bat is a stronger seed disperser without checking the seed viability first .
B irds and bats seed dispersal 12 Seeds Traps For most of the seeds I was only able to iden tify them down to their familiy and genus , so it was difficult to determine precisely the po rtion of pioneer species among all the seed found in the samples. Nevertheless, the information about the seed genera can provide us some useful information about their natural history . According to records from past st udies, frugivorous bats in the N eotro pics were dispersing Piper species like P. auritum, P. amalago, P. hispidum and P. nitidum , which are all pioneer shrubs that can grow bet ter in opening areas (Medellin & Osiris 1999, Fleming & Heithaus 1981, de Carvalho Ricardo 2013 , Standley 1937). Besid es , according to a study b y Murray in 1988, not only bats but also the black faced solitaire , a common species in Monteverde, can serve as the main dispersers of the Piper plants . Similar to bats dispersing Piper seeds, they were found to disperse seeds fr om the genus Witheringia , and other see ds from the Solanaceae family , which are all pioneer shrub species, in the tropic forests (de Carvalho Ricardo et al . 2013, Medellin & Osiris 1999) . Carollia perspicillata were found to be the primary consumer and dis perser of Piper seeds (Fleming & Orsiris 1981). In the samples I collected, a large number of Piper and Witheringia seeds were found in bat samples. Consider ing the prevalence of their primary dispersers, the frugivo rous bats (Appendix II), and the large n umber of seeds in each bat defecates, it's likely these two genera have a high pot ential to establish as pioneer plants in naturally disrupted areas in Monteverde. Noticeably, both in the bird fecal samples and the seed traps I found a relatively large nu mber of Myrsine coriacea seeds. M. coriacea is a pioneer plant species that has a high preference in the environment of a gap phase , which is an open area in the forest caused by tree falls (Klein 1980, Reitz et al . 1979). The plant has a wide range of see d shadow extended to diverse types of habitat , since multiple bird species help disperse the seeds (Table 1, Coleman 2015, Pinheiro & Carmo 1993) . The presence of multiple seed dispersers gives the plant a higher chance to reach the naturally disrupted ope n areas. The pres ence of the M. coriacea tree can initiate and accelerate the new v egetation succession growth by providing perches, shelters , and food sources for more seed dispersers , and thus encourage them to bring more seeds to the area where M. coria cea grow ( Medellin & Osiris 1999, Begnini & Castellani, 2013). Topics for Future Studies Some future research topics are the seed dispersal situation in other times of the year, the sources of the seeds that got dispersed, the viability of the seeds that got dispersed, and the overlap between the dispersed seeds and the seedlings grow th in the naturally disturbed area. Because the seeds get dispersed in different times of the year tend to thrive very different due to the different fruiting plants present and the different c omponents in the animal community (Fleming & Heithaus 1981), f uture studie s can replicate this study in other months to see the variance in the number and the diversity of t he seeds that get dispersed in different times of the year . Also , researchers can go to the naturally disrupted areas and record the species of the seedlings. Any overlap between the seedling species and the seed species dispersed by birds or bats provides clues of how aerial animal seed dispersal contribute to the veg etation succession in these areas. In conclusion , the species richness of the seed dispersers contribute to the richness of seed species they can disperse. Both the bats and birds, which include migratory and resident species, are essential in providing s eed dispersal services to the local plant community in
Bird s and bat s seed disp ersal 13 Monteverde. After the storm, the presence of these dispersers can effectively increase the resilience of habitats by accelerating the plant succession process by dispersing seeds of pioneer species. An d from the abundance of M. coriacea found in the samples and the fact that I also found the species in the seed traps, we can foresee the active role M. coriacea play in this new vegetation succession. ACKNOWLEDGEMENT S I would have been unable to compl ete this study without the help of so many people. I want to thank my primary advisor AndrÂŽs Camacho and secondary advisor Federico Chinchilla , for helping me form the idea of this study, giving advice and helping out when ever I experienced difficulties, a nd finally help me translate my title and abstract in Spanish. I want to thank Luisa Moreno and Federico Chinchilla for kindly letting me accompany the mist netting project for birds during the day, and the mist netting for bats during the night. I want to thank Mr. Rodrigo Solano for using his precious time to help me identify all of the seeds I found in the samples and traps. Thanks to the Monteverde Institute and the Biological Station for letting me use their space and facilities and thanks to Luisa aga in for letting me use the lab in the Monteverde Institute . Thanks to all of my peers and friends , who gave me great encouragement . I want to give special thank to John for giving me the inspiration of doing a project on seed dispersal . Thanks to Nicole and Shilah, who let me accompany them during the bat mist netting nights over the course of two weeks. Thanks to Mackenzie for willing to do a leaf pair project with me even when I was at the mist net s all day . Special thanks to Eric for peer reviewing my pap er and gave me extremely helpful advice it. Finally, I am so grateful for having Frank as well as all the EAP faculty members as my instructor s, for them giving me all the curiosity and passion in pursuing my interest in Biology. LITERATURE CITED Aguilar Garavito, Mauricio, Luis Miguel Renjifo, and Jairo PÂŽrez Torres. "Seed dispersal by bats across four successional stages of a subandean landscape." Biota Colombiana 15.2 (2014): 87 101. Coleman,J. (2015). Diversity of Black Guan's seed consumption and its digestive system's effect on seeds' germination capacity in Monteverde, Costa Rica. Tropical Ecology and Conservation Council on International Educational Exchange , Fall 2015 de Carvalho Ricardo, M. C., Uieda, W., Fonseca, R. C. B., & Rossi, M. N. (2014). Frugivory and the effects of ingestion by bats on the seed germination of three pioneering plants. Acta oecologica , 55 , 51 57. Dinerstein, Eric. "Reproductive ecology of fruit bats and the seasonality of fruit production in a Costa Rican cloud forest." Bi otropica (1986): 307 318. EFE. "La tormenta tropical Nate deja al menos 23 muertos y 27 desaparecidos en CentroamÂŽrica" RTVE, 6 Oct. 2017, http://www.rtve.es/noticias/20171006/lluvias asociadas tormenta tropical nate dejan menos 23 muertos 27 desaparecidos centroamerica/1626235.shtml
B irds and bats seed dispersal 14 Fleming, T.H. 1986. Opportunism versus specialization: the evo lution of feeding strategies in frugivorous bats. Pp. 105 118, in Frugivores and seed dispersal (A. Estrada and T.H. Fleming, eds.). Springer, New York, 392 pp. Fleming, Theodore H., and E. Raymond Heithaus. "Frugivorous bats, seed shadows, and the structu re of tropical forests." Biotropica (1981): 45 53. GarcÂ’a, D. et al. 2013. Functional heterogeneity in a plant Ã frugivore assemblage enhances seed dispersal resilience to habitat loss. Ã Ecography 36: 197 Ã 208. Guariguata, Manuel R. "Landslide disturbance an d forest regeneration in the upper Luquillo Mountains of Puerto Rico." The Journal of Ecology (1990): 814 832. Lawton, Robert O., and Francis E. Putz. "Natural Disturbance and Gap Phase Regeneration in a Wind Exposed Tropical Cloud Forest." Ecology , vol. 6 9, no. 3, 1988, pp. 764 Ã 777. Henderson, C. L., & Adams, S. (2010). Birds of Costa Rica: a Field Guide (Vol. 64). University of Texas Press. Klein, R. M. 1980. Ecologia da flora e vegetacÃ¼ Ã·ao do Vale do ItajaÂ«Ãµ (continuacÃ¼ Ã·ao). Sellowia 32:165 Ã 389. Medel lin, Rodrigo A., and Osiris Gaona. "Seed dispersal by bats and birds in forest and disturbed habitats of Chiapas, Mexico." Biotropica 31.3 (1999): 478 485. "Monteverde September weather." AccuWeather , https://www.accuweather.com/en/cr/monteverde/1179698/september weather/1179698?monyr=9/1/2017&view=table . Accessed 5 December 2017. Murray, K. G. 1988. Avian seed dispersal of three neotr opical gap dependent plants. Ecological Monographs 58:271 298. Pinheiro, A. L. & Carmo, A. P. T. 1993. ContribuicÃ¼ Ã·ao ao estudo tecnolÂ«ogico da Canela azeitona, Rapanea ferruginea (Ruiz e Pav.) Mez, uma espÂ«ecie pioneira. I. CaracterÂ«Ãµsticas anatÃ¶omicas da madeira. CiÃ¶encia Florestal 1:121 Ã 145. Reid, F. (1997). A field guide to the mammals of Central America and Southeast Mexico . Oxford University Press. Reitz, R., Klein, R. M. & Reis, A. 1979. Madeiras do Brasil: Santa Catarina. Lunardelli, FlorianÂ«opo lis. 320 pp. Robertson, A.W., Trass, A., Ladley, J.J., Kelly, D., 2006. Assessing the benefits of frugivory for seed germination: the importance of the deinhibition effect. Funct. Ecol . 20, 58e66. Sato, T.M., Passos, F.C., RodrÂ’guez ! PÂŽrez, Javier, et al. "Seed dispersal by changing frugivore assemblages: a mechanistic test of global change effects." Oikos 126.5 (2017): 671 681. Schleuning, M. et al. 2015. Predicting ecosystem function from biodiversity and mutualistic networks: an ex tension of traitbased concepts to plant animal interactions. Ã Ecography 38: 380 Ã 392. Standley, P. C. 1937. Flora of Costa Rica. Publications of the Field Museum of Natural History, Botanical series 18. " MoSI: Monitoring Neotropical Migrants in Winter ." T he INSTITUTE for BIRD POPULATION , https://www.birdpop.org/pages/mosi.php . Accessed 1 5 December 2017. T homas, D, W. 1984. Fruit and energy intake budgets of frugivorous bats. Physiol. Zoo!. 57: 457 467. 1991. On fruits, seeds and bats. BATS 9(4): 8 13 Walke r, Lawrence R., et al. "Ecosystem development and plant succession on landslides in the Caribbean." Biotropica (1996): 566 576.
Bird s and bat s seed disp ersal 15 Wenny, D.G. "Black guans and seed dispersal in costa rica". The Cracid Newsletter 2 (1993): 13. Wenny, D.G. 1998. "Seed dispersa l, seed predation, and seedling recruitment of a neotropical montane tree". Ecological Monographs 70 (1998): 331 51. Wenny, D.G. and Levey, D.J. "Directed seed dispersal by bellbirds in a tropical cloud forest". Proceedings of the National Academy of Scien ces of the United States of America 95 (1998): 6204 6207 Wheelwright, N. T., & Orians, G. H. (1982). Seed dispersal by animals: contrasts with pollen dispersal, problems of terminology, and constraints on coevolution. The American Naturalist , 119 (3), 402 4 13. APPENDIX Appendix I : The family of the bird caught in the mist net, its species, its diet, whether it is a migrant or resident, number of the individual in this species, and what percent does this species account for the total number of captures. F amily Bird Species Diet Migrant or Resident n Percent Captured Emberizidae Chestnut capped Brush Finch ( Arremon brunneinucha ) I R 3 3.13 White eared Ground Sparrow ( Melozone leucotis ) I R 1 1.04 Common Chlorospingus ( Chlorospingus flavopectus ) O R 2 2 .08 Furnariidae Olivaceous Woodcreeper ( Sittasomus griseicapillus ) I R 5 5.21 Ruddy Woodcreeper ( Dendrocincla homochroa ) I R 4 4.17 Spotted Barbtail ( Premnoplex brunnescens ) I R 4 4.17 Spotted Woodcreeper ( Xiphorhynchus erythropygius ) I R 1 1.04 W edge billed Woodcreeper ( Glyphorynchus spirurus ) I R 1 1.04 Momotidae Blue crowned Motmot ( Momotus coeruliceps ) O R 3 3.13 Parulidae Golden crowned Warbler ( Basileuterus culicivorus ) I R 8 8.33 Kentucky Warbler ( Geothlypis formosa ) I M 1 1.04 Ovenbir d ( Seiurus aurocapilla ) I M 6 6.25
B irds and bats seed dispersal 16 Slate throated Redstart ( Myioborus miniatus ) I R 2 2.08 Wilson's Warbler ( Cardellina pusilla ) I M 1 1.04 Thamnophilidae Plain Antvireo ( Dysithamnus mentalis ) I R 3 3.13 Slaty Antwren ( Myrmotherula schisticolor ) I R 4 4.17 Trochilidae Green Hermit ( Phaethornis guy ) N R 3 3.13 Magenta throated Woodstar ( Calliphlox bryantae ) N R 1 1.04 Stripe tailed Hummingbird ( Eupherusa eximia ) N R 3 3.13 Troglodytidae Plain Wren ( Cautorchilus modestus ) O R 2 2.08 Rufous and white Wren ( Thryophilus rufalbus ) I R 2 2.08 White breasted Wood Wren ( Henicorhina leucosticta ) I R 1 1.04 Turdidae Black faced Solitaire ( Myadestes melanops ) O R 2 2.08 Black headed Nightingale Thrush ( Catharus mexicanus ) O R 2 2.08 Orange billed N ightingale Thrush ( Catharus aurantiirostris ) O R 2 2.08 Swainson's Thrush ( Catharus ustulatus ) O M 3 3.13 Wood Thrush ( Hylocichla mustelina ) O M 9 9.38 Tyranidae White throated Spadebill ( Platyrinchus mystaceus ) I R 2 2.08 Yellowish Flycatcher ( Empi donax flavescens ) I R 2 2.08 Olive stripped Flycatcher ( Mionectes olivaceus ) O R 13 13.54 Total 96 100 Appendix II : The family of the bat caught in the mist net, its species, its diet, number of the individual in this species, and what percent do es this species account for the total number of captures. Bat Family Bat Species Diet n Percent Captured Phyllostomidae Artibeus lituratus F 1 7.14
Bird s and bat s seed disp ersal 17 Artibeus toltecus F 2 14.29 Carollia perspicillata F 2 14.29 Carollia sowelli F 1 7.14 Hylonycteris underwoodi N 2 14.29 Micronycteris schmidtorum F 1 7.14 Sturnira ludovici F 4 28.57 Vespertilionidae Myotis pilosatibialis I 1 7.14 Total 14 100