VERTEBRATE COMMUNITY CHANGES ACROSS A 3200M AMAZON-TO- ANDES GRADIENT: COMPOSITION, STRUCTURE, AND OCCUPANCY
BY
DANIEL A. LOUGH
A Thesis Submitted to the Graduate Faculty of
WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCES
in Partial Fulfillment of the Requirements
for the Degree of
MASTER OF SCIENCE
Biology
December, 2017
Winston Salem, North Carolina
Approved By:
Miles R. Silman, Ph.D., Advisor
William E. Conner, Ph.D., Chair
Todd M. Anderson, Ph.D.
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ACKNOWLEDGEMENTS From the start, I would like to thank my advisor, Dr. Miles Silman, for his insightful guidance and constant enthusiasm throughout this process. I’d also like to thank the members of my committee, Dr. William Conner and Dr. Michael Anderson, for lending their time and perspective to this project. I’ve also benefited from the guidance and support of the entire Silman Lab: William Farfan Rios, Cassie Freund, Rachel
Hillyer, Jorge Cabellero Espejo, Max Messinger, and Jared Beaver. I am indebted to Dr.
Russell Van Horn, Dr. Nicholas Pilfold, and Dr. Mathias Tobler at San Diego Zoo
Global’s Institute for Conservation Research for their logistical and methodological support throughout this project. I owe a great deal of gratitude to Leydi Vanessa Aucacusi
Choque, Ricardo Vivanco, and Fredy Martin Guizado for their assistance in the field and their many hours of hard work. I would like to thank my undergraduate researchers that assisted me in classifying the thousands of camera trap photos: Rebecca Wiebki, Kimiko
Morris, Zachary Taylor, Kyla Mathon, Kristin Lanier, Nicholas Mouser, and Kiley Price.
I would also like to thank SERNANP-Manu and the staff at Manu National park, for permitting this project. Funding for this research came through the North Carolina
Academy of Science’s Bryden Grant, Wake Forest University’s Vecellio Grant, and the
Paul K. and Elizabeth Cook Richter Memorial Fund. I am gracious to the researchers at the Amazon Conservation Association and the Andes Biodiversity and Ecosystem
Research Group for their logistical support throughout this project. I would also like to thank my family and my fiancée for their constant love and support throughout this process. Finally, I would like to thank the faculty, staff, and graduate students of the Wake
Forest Biology Department for their support throughout this degree.
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TABLE OF CONTENTS
CHAPTER 1
MAMMAL AND BIRD DISTRIBUTIONS ALONG A 3200M ANDES-TO-AMAZON
GRADIENT IN MANU NATIONAL PARK, PERU
ABSTRACT……………………………………………………………………………....1
INTRODUCTION………………………………………………………………………...2
METHODS……………………………………………………………………………….4
Study Area………………………………………………………………………..4
Camera Deployment………………………………………………………………6
Elevational Range Data and Photographs…………………………………………7
Analysis……………………………………………………………………………9
RESULTS…………………………………………………………………………………9
Birds……………………………………………………………………………...9
Mammals…………………………………………………………………………17
DISCUSSION……………………………………………………………………………24
Birds……………………………………………………………………………...24
Mammals…………………………………………………………………………25
Conservation Implications……………………………………………………….31 iv
LITERATURE CITED…………………………………………………………………..34
CHAPTER 2
SEED SURVIVAL AND GRANIVORE COMMUNITY CHANGES ALONG A 3.9KM
TROPICAL ELEVATIONAL GRADIENT
ABSTRACT……………………………………………………………………………...43
INTRODUCTION……………………………………………………………………….44
Vertebrate Functional Traits and Changes in Plant-Animal Interactions………..46
Camera Traps: Novel Approach to Documenting Seed Mortality….……………47
METHODS………………………………………………………………………………48
Study Area……………………………………………………………………….48
Study Species…………………………………………………………………….49
Camera Design and Seed Arrays………………………………………………...51
Analysis…………….……………………………………………………………55
RESULTS………………………………………………………………………………..57
Seed Predator Community and Diversity………….…………………………….57
Seed Survival…………………………………………………………………….59
Occupancy of Granivores………………………………………………………..69
DISCUSSION……………………………………………………………………………80 v
Granivore Species Richness, Seed Survival and Occupancy across the Elevational
Gradient……………………………………….……………..…………………...80
Seed Survival and Seed Defenses………..………………………………………81
Occupancy of Granivores and Seed Survival……………………………...…….83
Further Studies…………………………………………………………………...86
LITERATURE CITED…………………………………………………………………..89
APPENDIX 1…………………………………………………………………………...100
CURRICULUM VITAE………………………………………………………………..107
vi
LIST OF FIGURES
FIGURES
Chapter 1 1. Map of camera stations in Manu National Park, Peru………………………….....5
2. Elevational distribution shifts of birds…………………………………………...13
3. Differences in avian species richness across elevational gradient……………….15
4. Differences in terrestrial-foraging avian species richness across the elevational
gradient……………………………………………..……………………………16
5. Elevational distribution shifts of mammals……………………..……………….20
6. Differences in mammalian species richness across elevational gradient ……….23
7. Photograph of Andean white-eared opossum (Didelphis pernigra)….………….27
8. Photographs of mountain coatis (Nasuella sp.)………………………………….28
9. Differences in mammalian predator richness ………………………….……...... 30
10. Differences in mammalian seed disperser richness ……………………………..32
Chapter 2 1. Granivore species richness across the elevational gradient……………………...50
2. Camera station design..…………………………………………...... 52
3. Seed array design………………………………………………………………...54
4. Granivore detections……………………………………..………………………58
5. Granivore elevation distributions…………………………………..…………….60
6. Proportion of seeds removed over the elevational gradient……………………...61
7. Proportion of seeds removed per granivore taxa………………………………...63 vii
8. Seed survival over the elevational gradient…..……..….………………………..64
9. Time to removal of all three seed species per elevation……………………...... 67
10. Detection probabilities of granivore taxa over the elevational gradient………...70
11. Detection probabilities of granivore guilds over elevational gradient…………..72
12. Detection probabilities of granivore guilds with slope………………………….77
13. Detection probabilities of granivore guilds with aspect…………………………78
14. Detection probabilities of granivore guilds with habitat…………………………79
15. Mammalian predator detection probabilities over the elevational gradient……...85
16. Proportion of all removed seeds by granivores………………………………….88
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LIST OF TABLES
TABLES Chapter 1 I. Bird species documented outside their previous range………………………11
II. Birds with range extensions broken into guilds……………………………...14
III. Mammal species documented outside previous range……………………….18
IV. Detected mammals and their guilds and body sizes…………………………21
Chapter 2
I. Covariates for Cox Proportional Hazard Model……...………………………65
II. Best Cox Proportional Hazard Models……...………..……………………...66
III. Granivore occupancy and detection probability…………………………….71
IV. Best occupancy models per granivore………………………………………73
V. Effects of individual covariates on occupancy of granivores……………….75
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CHAPTER 1
MAMMAL AND BIRD DISTRIBUTIONS ALONG A 3200M ANDES-TO-AMAZON
GRADIENT IN MANU NATIONAL PARK, PERU
ABSTRACT Conservation planning depends heavily on understanding current species distributions. However, most Neotropical vertebrate distributions are poorly known and depend on field survey techniques which may not capture the full extent of an animals’ range. Here we present findings from two camera surveys in 2013 and 2016 conducted in and near Manu National Park, Peru. In 2013, 53 camera traps were installed between
3693 -1271 m a.s.l to identify both mammal and bird species along two parallel elevational transects composed of tropical montane cloud forest. In 2016, we replicated and extended the survey along one transect, setting 80 cameras from 3578 to 519 m a.s.l.
We use these findings in conjunction with existing range hypotheses to assess (1) if there are major distribution changes (≥100 m, ~0.5 deg C) for mammal and bird species and whether there is a pattern among guilds and (2) quantify whether species richness across the elevational gradient changes as a result of new range estimates. Of the 83 taxa of identifiable birds, 18% had their distributions increased by ≥100 m with an average of two novel species per elevation. In contrast, of the 54 taxa of mammals detected, 44% had their distributions extended by ≥100 m, with most taxa acting as either predators or seed dispersers, with an average of six novel species per elevation sampled. These findings are crucial for expanding our understanding of tropical communities and what is needed to better conserve them.
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INTRODUCTION
Understanding current species distributions is crucial for biodiversity conservation and predicting community responses to anthropogenic climate change
(Feeley and Silman, 2011). It has been well documented that temperate species will move latitudinally in response to dramatic variation in climate to find more suitable climates in which to survive (von Post 1916; Davis 1969). However, because of shallow temperature gradients at low latitudes, tropical species tend to move altitudinally, rather than latitudinally, to find more suitable climates in which to survive (Janzen 1969; Forero-
Medina et al. 2006; Colwell et al. 2008; Lutz et al. 2013). Therefore, knowledge of the current elevational ranges of tropical species is vital to predicting future community shifts and creating adaptive conservation management plans (Ahumada et al. 2013; Fleming et al. 2014).
Though understanding elevational distributions is central to conservation and basic understanding of ecosystem function, little is known about the current elevation and geographic ranges of many Neotropical animals, especially in the tropical montane cloud forest (TMCF) (Ledo et al. 2012; Piana & Luna 2016). The Tropical Andes is a global biodiversity hotspot (Myers et al. 2000), made up of the eastern slope of the Andes and adjacent Amazonian lowlands. The Tropical Andes hosts the highest vertebrate endemism of all global hotspots with 1567 species: 43% birds, 4% mammals, and 53% herptefauna (Myers et al., 2000). However, due to its remoteness and rough terrain, little is known about the basic ecology of many of the species (Foster 2001; Malhi et al. 2010). 3
What is known about distributions of the mammals and bird species in the
Tropical Andes comes from sampling techniques that may give inaccurate information.
For example, most mammal surveys in this habitat have used live-trapping-which focus on the smallest mammalian species (Sahley et al. 2016) and rely heavily on eyewitness accounts or museum voucher specimens for larger mammal presence/absence (e.g. Solari et al. 2006). Birds are probably the best studied group of vertebrates in the tropical montane cloud forest (TMCF) (Terborgh 1977; Forero-Medina et al. 2006; Jankowski et al. 2012), but even within this well-studied taxon, the rarer and cryptic species that forage terrestrially remain under-detected in traditional bird counts (Diefenbach et al. 2003).
Motion-activated, infrared camera traps allow researchers to monitor and catalogue species that are otherwise cryptic, specifically nocturnal mammals and terrestrial birds (Balme 2009; Tobler et al. 2008), and have the potential to alleviate many of these biases and update our view of vertebrate ranges. Camera traps are an affordable means of cataloguing wildlife in an area, they also allow for replication of results, minimize sampling error, and expand both the spatial and temporal scale of sampling
(Ahumada et al. 2013; Hamel et al. 2013). Camera traps provide insight on community composition, species diet, daily activity, habitat preference, and inter and intra-specific interactions (Tobler et al. 2008; Flemming et al. 2015; Anderson et al. 2016). They also function without human presence, thus allowing researchers to capture more natural animal behavior (Hamel et al.2013) and minimize the sampling effort required in traditional line transects, which can be subject to bias (Ferreguetti et al. 2017). Camera traps can also monitor large areas for long periods of time, allowing for estimates of the 4 extent of the total vertebrate community (Ahumada, et al., 2012; Anderson et al., 2016), thus giving us better estimates for species distributions.
In this study I present my findings from two camera surveys designed to identify mammals and birds inhabiting the eastern slope of the Tropical Andes. In 2013, 53 camera traps were installed along two parallel elevational transects composed of primarily TMCF within Manu National Park. In 2016, I replicated and extended the survey along one of the transects, setting up 80 cameras from 3500 m to 500 m and extending into protected areas alongside the park’s boundaries, encompassing not only the entire TMCF but also sub montane and lowland rainforest ecosystems. Here we use these data in conjunction with existing range hypotheses to (1) determine if there are any large distribution changes in elevational range hypotheses, (2) for those taxa with large
(≥100m, ~0.5°C) changes in range hypotheses, explore simple predictors such as foraging guild or body size that relate to the degree of range expansion, and (3) document how trophic structure and species richness across the elevational gradient changes with updated range predictions.
METHODS
Study Area
Camera surveys were conducted in and near the UNESCO World Heritage Site of
Manu National Park, Peru (Figure 1). The 2013 survey was conducted along parallel montane transects within Manu National Park in primary forest, with one in the
Kosñipata Valley (13°S, 71°E) and the other in the Callanga Valley (12°S, 71°E) from late June through early December. The Kosñipata transect is a 17km ridge descending 5
Figure 1:The maps depict the camera locations in 2013 and 2016. Sampling in 2013 included both the Callanga and Kosñipata valleys and were placed within the TMCF.
Sampling in 2016 was done only in the Kosñipata valley but extended down into the lowland tropical rainforest.
6 from 3693 m to 1831 m and contains 12 botanical collection plots in primary TMCF
(www.andesconservation.org). The Callanga transect has a long history of human activity including selecative logging and has been occupied by people since Incan times. Callanga camera placement sites ranged between high as 3170 m-1271 m a.s.l. and encompassed the breath of the TMCF habitat. Mean temperatures range from 6°C at 3600 m to 20°C at
1200 m (Rapp & Silman 2012). Annual precipitation ranges from 2.4m at 3600 m to 5 m at the lowest extent, with the Callanga Valley being slightly drier due to orographic effects (Rapp & Silman 2012).
In 2016 the survey was repeated and focussed on the Kosñipata Valley, from late
May through early November. Cameras were placed in a subsample of elevations examined in 2013 (3500 m, 3400 m, 3200 m, 3000 m, 2400 m, and 2000 m) and extended to two sites lower in elevation (1750 m and 1500 m), encompassing the entire TMCF habitat within the valley. Cameras were also installed at the bottom of the valley at Villa
Carmen Biological Station at 500m and 750m sites to record species that reside in lowland forest. Both additional plots at 1500 m and 1750 m are examples of primary
TMCF while the Villa Carmen Sites were selectively logged nearly 20 years ago. Mean annual temperature in this survey varied from from 6°C at 3600 m to 24°C at 500 m
(Amazon Conservation Association 2011; Rapp & Silman 2012).
Camera Deployment
A total of 53 Bushnell MP Trophy Cameras were used in the 2013 study.
Thirty-two cameras were placed along the Kosñipata transect from 3693m to 1831m. The other 21 cameras were placed along the Callanga transect from 3082m to 1271m. The cameras were spaced approximately every 0.8km along the gradients. All cameras were 7 set to take three photos per detection; with three cameras along the Kosñipata transect set to take video. Each camera had a 1 second lapse between photos and sensitivity was set to high. Cameras on the Kosñipata transect were deployed from June-October 2013 while cameras on the Callanga transect were deployed from July- December 2013.
In 2016, 80 Bushnell MP Trophy Cameras were used in the Kosñipata Valley and installed in primary forest at elevations ranging from 3578m to 519m. Each camera site was set at predetermined elevations where major species and community turnovers occurred as determined by Solari et al. (2006) and Walker et al. (2006): 3400 m, 3200 m,
3000 m, 2400 m, 2000 m, 1750 m, 1500 m, 750 m, and 500 m. Each camera station contained two cameras facing the same direction, with one oriented parallel to the ground and one oriented 45° down at the ground at approximately 1m and 0.5m height, respectively. The dual camera orientation was used in order to better identify small mammals and birds, which can have a lower probability of triggering sensors. At five of the elevations (3400 m, 3000 m, 2000 m, 1500 m, and 500 m), six additional camera stations were installed to monitor seed removal experiments. Each of these six camera stations were set up with an average distance of 30m between one another at each site.
All cameras were set to take three photos per detection and the sensitivity was set to high.
Cameras were deployed from May 2016-November 2016.
Elevational Range Data and Photographs
Mammals: In order to compare observed mammal distributions to existing hypotheses I used Solari et al. (2006), which previously listed the elevational ranges of mammals in Manu National Park based on eyewitness accounts and small mammal trapping campaigns. I also compared any range extensions for each species to elevational 8 ranges recorded over the entire distribution of a species based on data from the open access Global Biodiversity Information Facility (GBIF: http://www.gbif.org/). GBIF is the largest online repository of biological collection and observation records, containing records from natural history museums across the globe. Although a number of smaller mammals, like rodents (largely Cricetidae) and opossums (Didelphidae) were photographed within the two camera surveys (Appendex 1), exact species identification is very difficult based on the extreme diversity of the two families within the park (N= 52 and N=12 species, respectively) and the lack of photographically distinguishable charactreistics. Based on previous trapping campaigns throughout Manu National Park and elsewhere in Peru, these two groups have had minimal range extensions (Solari et al.
2006; Medina et al. 2012). Photographs of medium and large mammals at each site were identified with pictures from other camera surveys and photographs stored on ARKive
(ARKive: http://www.arkive.org/ ) and their elevational ranges were compared to Solari et al. (2006). Mammals with range extensions were then separated into ecological guilds
(i.e. ecological roles, dietary niches, daily activity, and locomotion preference) and body size to see if these factors may explain why these particular species had range extensions
(Eisenberg and Redford, 1999).
Birds: I did a similar process with birds but compared my observations with distribution predictions made by Walker et al. (2006). Walker et al. (2006) created these range predictions by using the traditional censusing methods of vocalizations, mist- netting, and eyewitness encounters, thus forming the basis for my range extension predictions for birds. I then compared these elevational range hypotheses to distribution- wide elevatioal ranges based on collections stored on GBIF. Photographs of birds were 9 compared to illustrations in Schulenberg et al. (2007) and from photographs stored in
ARKive. The birds with range extensions were then broken up into two guilds (diet and foraging activity) and body classes (Schulenberg et al. 2007; Cornell Lab of Ornithology
Neotropical Birds 2017) to see if there were any major patterns among guilds and body size that may explain these range extensions. For both birds and mammals any range extension of 100m or more was considered significant as this represents an average temperature change of 0.5°C given the lapse rate of the region (Lutz et al. 2013).
Analysis
For those species with distribution changes, I used a χ2 test on each functional guild and body class to assess if there were any significant differences among the observed distribution changes for birds and mammals. The χ2 test was done using R
3.3.1 (R working group 2017) with the built in function chisq.test. The χ2 test was chosen due to small sample size but it also fit the criteria of our null hypothesis; that there was no difference between guilds or body sizes of species with distribution changes. Alpha was set to 0.05.
RESULTS
The 53 cameras in 2013, were deployed for 6,395 camera days resulting in 32,854 pictures of animals and 65,839 pictures in total (32,985 false positives). The 80 cameras in 2016, were deployed for 9,254 camera days resulting in 121,464 pictures of animals and 345,498 pictures in total (224,034 false positives). Together, the surveys documented
83 identifiable taxa of birds from 26 families, with 79 taxa identifiable to species and four taxa identifiable only to genus (Appendix 1). The surveys also documented 54 10 identifiable taxa of mammals-belonging to 21 families, with 43 identifiable to species and
11 taxa to genus (Appendix 1).
Birds
I recorded 15/83 taxa of birds (18%) outside of their previously documented ranges within the park by more than 100 m in elevation. Of the total detections of these
15 species, only 8.6% (44/510) were outside of their ranges predicted by Walker et al.
(2006; Table I). However, when examining the global records for these species, only 8%
(7/83) of these species were outside their previous documented ranges (Table I).
Distributions of these species increased from 100 m, for the White-throated Antpitta
(Grallaria albigula), to 600 m, for the Wattled Guan (Aburria aburri), with a mean distribution change of 283± 178.12 m across all taxa (Figure 2). Most changes were increases but two mid-montane bird species, the White-throated Quail-Dove (Geotrygon frenata) and the Black Tinamou (Tinamus osgoodi), had notable downward elevational distribution changes both for Manu National Park and globally (Table I).
Broken into guilds (Table II), the most significant difference for distribution changes was foraging type ( χ2= 11.27, df=1, p=0.001) with a disproportionate number of range extensions belonging to terrestrial foragers (Table II). Neither avian diet (χ2=
0.067, df=1, p=0.796) nor body size class ( χ2= 1.33, df=4, p=0.856) was assosciated with range extensions. Avian species richness changed by an average of two species per elevation with new range hypotheses, although this had little effect on the overall community diversty at each elevation (Figure 3), even when considering species richness among terrestrial feeding birds (Figure 4). 11
Table I: Table of bird species that were documented outside their current range by
≥100m and detections outside of their previously documented ranges in the camera
surveys with SDZG and ABERG. Species are arranged phylogenetically and within
genera, arranged alphabetically.
Common Scientific Elevational Elevational Elevational # of # of % of Name Name Range by Range Range By Detections Detections Detections Walker et Based on GBIF of Species Outside of Outside of al., 2006 Cameras Range Range
Brown Crypturellus 450-2500m 537-3096m 450-2900m 243 1 0.41 Tinamou obsoletus
Hooded Nothocerus 1600- 1520- 2000- 81 1 1.2 Tinamou nigrocapillus 3200m 3351m 3200m
Taczanowski’s Nothoprocta 3200m 3451m 2700- 1 1 100 Tinamou taczanowskii 4000m
Black Tinamus 900-1350m 750-1562m 900-1400m 15 13 87 Tinamou osgoodi
Gray Tinamou Tinamus tao 250-1300m 750m- 120-1900m 12 2 16.7 1534m
Wattled Guan Aburria aburri 650-1600m 1520-2200 700-2200m 2 1 50
White- Geotrygon 700-2850m 528-2850m 700-3000m 55 2 3.6 throated frenata Quail-Dove
White-backed Pyriglena 500-1850m 1492- 500-2200m 22 12 55 Fire-eye leuconata 2110m
White- Grallaria 1150- 1150- 800-3200m 6 2 33 throated albigula 2100m 2200m Antpitta
Rusty-breasted Grallaricula 2600- 2600- 600-3350m 2 1 50 Antpitta ferrugineipectus 3250m 3460m
Rufous- Ochthoeca 2500- 3560m 2000- 1 1 100 breasted Chat- rufipectoralis 3450m 3600m tyrant
Slaty-back Catharus 1500- 1500- 600-3250m 2 1 50 Nightengale- fuscater 2850m 3170m Thrush
Glossy-black Turdus 1400- 2507- 1400- 10 5 50 Thrush serranus 3200m 3461m 3250m
Stripe-headed Arremon 2500- 2000m- 2000m- 42 1 2.4 Brush-Finch torquatus 3250m 3200m 3300m 12
Common Scientific Elevational Elevational Elevational # of # of % of Name Name Range by Range Range By Detections Detections Detections Walker et Based on GBIF of Species Outside of Outside of al., 2006 Cameras Range Range
Black-faced Atlapetes 1400- 1898- 1500- 20 1 5 Brush-Finch melanolaemus 3200m 3453m 3000m
Total #of 514 45 8.75 Detections:
13
Figure 2: Elevational range hypotheses of 15 avian species detected outside their previously documented ranges. The pink lines are the hypothesized minimum and maximum elevational distributions by Walker et al. (2010) (previous). The blue lines are the hypothesized minimum and maximum elevational distributions based off of our camera survey (observed) and Walker et al.’s hypotheses. Species are arranged in increasing central tendancy of observed distributions (blue points).
14
Table II: The birds with range extensions of ≥100m that were detected during the camera surveys with their diet, foraging activity, and height (cm). Species are arranged phylogenetically and within genera, arranged alphabetically.
Common Name Scientific Name Diet Foraging Height Activity
Brown Tinamou Crypturellus Herbivore Terrestrial 24-27cm obsoletus
Hooded Tinamou Nothocerus Herbivore Terrestrial 33cm nigrocapillus
Taczanowski’s Nothoprocta Herbivore Terrestrial 33-36cm Tinamou taczanowskii
Black Tinamou Tinamus osgoodi Herbivore Terrestrial 40-46cm
Gray Tinamou Tinamus tao Herbivore Terrestrial 43-46cm
Wattled Guan Aburria aburri Herbivore Terrestrial 44-48cm
White-throated Geotrygon Herbivore Terrestrial 29.5- Quail-Dove frenata 32cm
White-backed Pyriglena Insectivore Terrestrial 17.5- Fire-eye leuconata 18cm
White-throated Grallaria Insectivore Terrestrial 18.5cm Antpitta albigula
Rusty-breasted Grallaricula Insectivore Terrestrial 10-11cm Antpitta ferrugineipectus
Rufous-breasted Ochthoeca Insectivore Aerial 12.5- Chat-tyrant rufipectoralis 13cm
Slaty-back Catharus Insectivore Terrestrial 17-18cm Nightengale- fuscater Thrush
Glossy-black Turdus serranus Insectivore Terrestrial 24-25cm Thrush
Stripe-headed Arremon Insectivore Terrestrial 15-17cm Brush-finch torquatus
Black-faced Atlapetes Insectivore Terrestrial 16-17cm Brush-Finch melanolaemus
15
Figure 3. Differences in the bird community species richness between range hypotheses of Walker et al., 2006, (solid line) and with our range hypotheses (dotted line).
16
Figure 4. Differences in terrestrial foraging bird community species richness between range hypotheses of Walker et al. (2006) (solid line) and our range hypotheses (dotted lines). Data on foraging habits was taken from Cornell Lab of Ornithology Neotropical
Birds (2017) and Schulenberg et al. (2007).
17
Mammals
Of the 53 photographed taxa of mammals documented on the cameras, 24 taxa had their elevational ranges extended by ≥ 100 m, with extralimital detections being 22% of total detections of these taxa (Table III). However, when compared to global records, only 18% (10/53) of these species were above the elevation reported in global records.
Records for tayra (Eira barbara) and bushdog (Speothos venaticus) are the highest global records by a substantial margin (Table III). Range increases from Solari et al. (2006) were from 125 m for the margay (Leopardus weidii), to 2620 m for the bushdog
(Spetheos venaticus), with a mean distribution change of 813±709 m in increased elevation across all taxa (Figure 5). Two small carnivores that had one record each, from one elevation, oncilla (Leopardus tigrinus) and long-tailed weasel (Mustella frenata), I found that they had much larger distributions which encompassed nearly the entire
TMCF (1266-3460m and 1920-3578m, respectively). Only the dwarf brocket deer
(Mazama chunyi) had a 200 m decrease in elevation (Table III).
When I examined these taxa with distribution changes among ecological guilds, neither ecological role ( χ2= 2.7, df=2, p=0.26) or dietary niche ( χ2= 4.33, df=3, p=0.23) were significant predictors of elevation range changes. Sixty-five percent of the mammals with distribution changes were nocturnal and 63% were terrestrial in behavior (Table IV) with neither being significant predictors of distribution changes ( χ2= 1.5, df=1, p=0.22 for both guilds). Body size was not a significant predictor of distribution changes ( χ2=
7.5, df=5, p=0.19). Species richness of non-volant mammals, with mass ≥100g, changed by an average of six species per elevation with these new range hypotheses with the largest changes occurring from 500-2200m (Figure 6). 18
Table III: Table of mammal species that were documented outside their current range by
≥100m and detections outside of their previously documented ranges in the camera
surveys with SDZG and ABERG. Species are arranged phylogenetically and within
genera, arranged alphabetically.
Common Scientific Previous Elevational Elevational # of # of % of Name Name Elevational Range Based Range By Detections Detections Detections Range on Cameras GBIF of Species Outside of Outside of Range Range
Common Didelphis 400-1920m 1266-2180m 120-2000m 9 2 22 Opossum marsupialis
Nine- Dasypus 380-1000m 521-1266m 150-1250m 13 1 8 banded novemcinctus Armadillo
Giant Priodontes 350-380m 537m 180-400m 2 2 100 Armadillo maximus
Giant Myrmecophaga 350-380m 500m 180-500m 1 1 100 Anteater tridactyla
Southern Tamandua 350-380m 521-1505 150-1000m 3 2 67 Tamandua tetradactyla
White- Cebus 350-400m 1289-1492m 35-2100m 2 2 100 fronted albifrons Capuchin
Bolivian Sciurus ignitus 350-600m 1266-1982m 150-2350m 12 12 100 Squirrel
Northern Sciurus 600-850m 1500m 150-850m 1 1 100 Amazon igniventris Red Squirrel
Lowland Cuniculus paca 350-1000m 521-1750m 140-1524m 259 30 12 Paca
Mountain Cuniculus 1920-3450m 1855-3560m 1920-3450m 398 4 1 Paca taczanowskii
Central Dasyprocta 350-1000m 1266-2200m 280-1200m 57 57 100 American punctata Agouti
Short-eared Atelocynus 350-450m 750m 180-762m 1 1 100 Dog microtis
Bush Dog Speothos 380m 3000m 180-380m 1 1 100 venaticus
Kinkajou Potos flavus 350-1460m 2102m 120-1524m 1 1 100 19
Common Scientific Previous Elevational Elevational # of # of % of Name Name Elevational Range Based Range Detections Detections Detections Range on Cameras Based on of Species Outside of Outside of GBIF Range Range
Tayra Eira barbara 350-1920m 521-3451m 190-2790m 44 19 43
Greater Gallictus 380m 380-1500m 210-1200m 1 1 100 Grison vittata
Long-tailed Mustela 3350m 1920-3560m 2050-3962m 21 20 95 Weasel frenata
Ocelot Leopardus 350-450m 521-750m 150-1738m 12 10 83 pardalis
Oncilla Leopardus 1460m 1266-3460m 120-3800m 31 20 65 tigrinus
Margay Leopardus 370-400m 521m 210-860m 1 1 100 weidii
Jaguar Panthera onca 350-1000m 1750m 160-3000m 1 1 100
Collared Pecari tajacu 350-450m 522-1500m 130-3000m 3 3 100 Peccary
Red Mazama 350-480m 521-750m 130-4000m 31 19 62 Brocket americana Deer
Dwarf Mazama 2450-3300m 2200-3351 1524-3350m 36 1 3 Brocket chunyi Deer
Total #of 941 212 22.45 Detections:
20
Figure 5: Elevational range hypotheses of 24 mammal species detected outside their previously documented ranges. The pink lines are the hypothesized minimum and maximum elevational distributions by Solari et al. (2006) (previous). The blue lines are the hypothesized minimum and maximum elevational distributions based off of our camera survey (observed) and Solari et al.’s hypothoses. Species are arranged in increasing central tendancy of observed distributions (blue points).
21
Table IV. The twenty-four mammals that need their ranges extended by at least 100m and the guilds that they belong too. Guild information was taken from both Eisenberg and
Redford, 1999, and The IUCN Red List. Species are arranged phylogenetically and within genera, arranged alphabetically.
Common Name Scientific Ecological Diet Daily Locomotion Weight Name Role Activity Preference
Common Didelphis Seed Omnivore Nocturnal Semi-Arboreal 1-1.5kg Opossum marsupialis Disperser
Nine-banded Dasypus Predator Omnivore Nocturnal Terrestrial 2.5-6.5kg Armadillo novemcinctus
Giant Armadillo Priodontes Predator Insectivore Nocturnal Terrestrial 18.7-35kg maximus
Giant Anteater Myrmecopha Predator Insectivore Nocturnal Terrestrial 33-41kg ga tridactyla
Southern Tamandua Predator Insectivore Nocturnal Semi-Arboreal 1.5-8.4kg Tamandua tetradactyla
White-fronted Cebus Seed Omnivore Diurnal Semi-Arboreal 2.9-3.4kg Capuchin albifrons Disperser
Bolivian Sciurus Seed Omnivore Diurnal Semi-Arboreal 183-212g Squirrel ignitus Predator
Northern Sciurus Seed Omnivore Diurnal Semi-Arboreal 480-665g Amazon Red igniventris Predator Squirrel
Lowland Paca Cuniculus Seed Herbivore Nocturnal Terrestrial 6-12kg paca Disperser
Mountain Paca Cuniculus Seed Herbivore Nocturnal Terrestrial 6-10kg taczanowskii Disperser
Central Dasyprocta Seed Herbivore Diurnal Terrestrial 3-5.2kg American punctata Predator Agouti
Short-eared Dog Atelocynus Seed Omnivore Diurnal Terrestrial 6.5-7.5kg microtis Disperser
Bush Dog Spetheos Predator Carnivore Diurnal Terrestrial 5-8kg venaticus
Kinkajou Potos flavus Seed Omnivore Nocturnal Semi-Arboreal 1.4-4.6kg Disperser
Tayra Eira barbara Seed Omnivore Diurnal Semi-Arboreal 2.7-7kg Disperser 22
Common Name Scientific Ecological Diet Daily Locomotion Weight Name Role Activity Preference
Greater Grison Gallictis Predator Omnivore Diurnal Terrestrial 1.5-3.8 vittata
Long-tailed Mustela Predator Carnivore Nocturnal Terrestrial 112-267g Weasel frenata
Ocelot Leopardus Predator Carnivore Nocturnal Terrestrial 8-16kg pardalis
Oncilla Leopardus Predator Carnivore Nocturnal Terrestrial 1.5-3.5kg tigrinus
Margay Leopardus Predator Carnivore Nocturnal Semi-Arboreal 2.6-4kg weidii
Jaguar Panthera Predator Carnivore Nocturnal Terrestrial 56-96kg onca
Collared Pecari tajacu Seed Omnivore Diurnal Terrestrial 16-27kg Peccary Predator
South American Mazama Seed Herbivore Nocturnal Terrestrial 24-48kg Red Brocket americana Disperser
Dwarf Brocket Mazama Seed Herbivore Nocturnal Terrestrial 8.5-13kg Deer chunyi Disperser
23
Figure 6. Differences in mammal community species richness between range hypotheses of Solari et al., 2006, (solid line) and our range hypotheses (dotted lines). Species above do not include members of the Order Chiroptera and have a mass greater than 100g.
24
DISCUSSION
Accurate distributional models are crucial for conservation, species management, and understanding ecosystem functions (Allouche et al., 2006; Feeley and Silman, 2011).
The results of this study show that nearly half of all detected mammals and nearly 1/5 detected birds had changes to their elevational distributions of ≥ 100m, corresponding to change in thermal niche of each of these species by more than 0.5°C (0.5°C-23°C, median temp of 15°C). Many medium-sized mammals, particularly predators, had elevational range increases of thousands of meters, fundamentally changing our views of the composition and function of high elevation mammal communities. Two important
“lowland” carnivores, bushdog (Speothos venaticus) and tayra (Eira barbara), had the highest current global record. Many of these mammalian distribution changes were of lowland rainforest inhabitants that were documented in the tropical montane cloud forest, showing a clear connection between the fauna of the two distinct but adjacent habitats.
Although it has been recognized that future management practices will need to connect lowland protected areas to upland protected areas (Ribeiro et al. 2016), tropical mammals and birds may already be inhabiting higher elevations and are in need of connectivity to montane forests at this present time.
Birds
Camera traps captured a biased sample of the avian community as most avian diversity in the tropics resides in canopy-dwelling species and we restricted our survey to the forest floor (Terborgh 1977). Although many arboreal species were detected by the cameras, there were overall fewer detections of them compared to ground dwelling birds.
In contrast, camera traps were useful in documenting the more reclusive terrestrial 25 species (Schulenberg et al., 2007) that may be overlooked in other sampling techniques.
One rare ground bird, the Black Tinamou (Tinamus osgoodi), had a high percentage of independent captures above its previously documented range. A study conducted by
Forero-Medina et al. (2006) showed that many bird species are moving upslope in response to climate change, but at a slower rate than what is needed to survive the predicted global temperature increase of 4°C by the end of this century. If these species are indeed foraging at these elevations, they may be more adept at surviving the predicted warming temperatures by moving upslope. However, we suggest that these distribution changes could be due to inadequet sampling, rather than species moving upslope in response to climate change.
Mammals
Unlike birds, the results of this study show that mammal distributions in Andean montane forests are poorly understood. Of the 53 taxa of mammals detected, 45% were detected outside of their previous ranges. This translates into 27% of known non-volant mammal taxa within Manu National Park having their distributions changed. This large percentage of observed mammals is likely due to biases in traditional sampling of the mammal community (i.e. line transects, footprints, eye witness testimonies, etc.).
However, although we recorded 85% of known terrestrial mammals within the park
(Appendix 1), our sampling technique was also biased towards predominantly terrestrial mammals. There maybe many more mammalian distribution changes in canopy species that were not-detected due to our sampling design. To add support to this idea, species that had large range extensions but few detections like kinkajou (Potos flavus), margay
(Leopardus weidii), and white-fronted capuchin (Cebus albifrons) are primarily arboreal. 26
To highlight our paucity about the mammal community in the TMCF of Manu
National Park we gathered photographic evidence for two mammal species previously not documented in the park. Medina et al. (2012) reported that the Andean white-eared opossum (Didelphis pernigra) was present in Manu National Park based on eyewitness testimonies. The large-bodied member of the Didelphidae family, 0.5-2.75kg, has been documented both in central Peru and northern Bolivia (IUCN RedList 2017) but the photograph of a sub-adult individual confirms its presence in Manu National Park (Figure
7). This was supported by the curator of Zoology at the Museo de Historio Natural, Lima, and Andean mammalogist Dr. Victor Pacheco. Mountain coatis (Nasuella sp.) have been documented in the northern Andes (Helgen et al. 2009) but photographs of several individuals and young from (1750-2054m) show that there is a population of these mammals inside Manu National Park (Figure 8). The nearest confirmed population is in southern Ecuador, ~1,783km from Manu National Park, although specimens have been collected throughout Central Peru (IUCN Redlist 2017). The identification of the genus was confirmed by Dr. Mirian Tsuchiya, a leading expert in Procyonid taxonomy and genetics at the Smithsonian Center for Conservation Genetics.
Most mammals (97%) had been previously documented within Manu but at much lower elevations than what was documented in our surveys (Emmons 1984; Srbek-Araujo
& Chiarello 2005), excluding the two new species (one new to Manu National Park and one new to science). This showcases the importance of the TMCF for mammalian diversity and it indicates these tropical mammals have broader temperature ranges than previously expected. Although many species had only one or a few detections above their previously documented range, species like the tayra (Eira barabara), Central American 27 agouti (Dasyprocta variegata), long-tailed weasel (Mustella frenata) and oncilla
(Leopardus tigrinus) were photographed frequently at different elevations, suggesting
Figure 7: Photograph of a sub-adult Andean white-eared opossum (Didelphis pernigra) at 3282m represents the first sighting of this species in Manu National Park. This photograph was co-confirmed by Dr. Victor Pacheco, Museo de Historio Natural, Lima.
28
Figure 8: Photographs of mountain coati at ~2000m. Photographs show a population of the Genera living in Manu National Park, Peru, that was confirmed by Dr. Mirian
Tsuchiya, Smithsonian Conservation Genetics.
29 that there are populations of these animals above or below their previously recognized ranges. Animals with small range sizes and poor dispersal capabilities (Sunquist et al.
1987; Brown et al. 2014; El Bizri et al 2016) like lowland paca (Cuniculus paca), common opossum (Didelphis marsupialis), and southern tamandua (Tamandua tetradactyla) are likely living at these higher elevations, despite being photographed less frequently. Other mammals, such as jaguar (Panthera onca), short-eared dog (Atelocynus microtis), white-fronted capuchin (Cebus albifrons), and giant armadillo (Priodontes maximus) had so few detections that we cannot know whether they are seasonal visitors or are permanent residents of these higher elevations (Defler 1980; Tobler & Powell
2013).
Most mammals detected outside of their previously documented ranges act either as predators or seed dispersers (44% and 39%, respectively; Table IV). These two guilds are important in ecosystem function as their behaviors influence both plant and animal species composition, abundance, and diversity (Bodmer 1991; Lazenby 2015). Predators have large effects on the abundance and composition of other species in communities
(Balme et al. 2009) and it was long thought that there was a large void in terestrial predator richness at higher elevations (Hillyer and Silman 2010). However, our camera trap findings show a diverse group of mammalian predators living at higher elevations that may continue to have top-down effects on the community (Figure 9), though understanding their abundances and biomass in addition to their simple occupancy is central to this question and remains unknown.
A diverse seed disperser community is also highly important to both biodiversity along this elevational gradient as well as ecosystem services like carbon storage. Feeley 30
Figure 9: Differences in mammalian predator community species richness between range hypotheses of Solari et al. (2006) (solid line) and our range hypotheses (dotted lines).
Species above do not include members of the Order Chiroptera and have a mass greater than 100g.
31 et al. (2011) showed that trees are moving upslope in response to climate change but at rates less than what is needed to keep up with current warming conditions. These mammals are essential to tree migration through moving seeds from lower elevations to higher ones via primary or secondary seed dispersal (Figure 10). Also, seed dispersal by mammals can play a role in carbon storage within ecosystems (Bello et al., 2015). Most of the largest trees in the forests, especially lowland forests, not only produce the largest seeds (Forget, 1991) but also store the most carbon (Bello et al., 2015). These trees heavily rely on animals, particularly medium-to-large sized mammals, to disperse their seeds (Bodmer, 1991; Hirsch et al., 2012) so a healthy seed disperser community greatly impacts plant community functions.
Conservation Implications and Future Directions
Defaunation in the tropics is a conservation concern, with direct human activities
(logging, over-hunting, etc.) and anthropogenic climate change the principle threats
(Harrison et al. 2013; Bello et al. 2015; Ribeiro et al. 2016). Many areas of the tropics are becoming void of seed dispersers and predators, thus endangering tropical communities (
Redford et al. 1992; Hairston et al. 2013). Here I show a diverse assemblage of species normally extirpated by human activities, critical for ecosystem services. It is crucial to set up networks to monitor animal communities over long periods which can take these data and incorporate them into meaningful action plans for conservation (Fleming et al. 2014;
Anderson et al. 2016). Several organizations have begun monitoring terrestrial mammals and birds throughout the tropics, but they only encompass a fraction of global tropical forests (TEAM Network 2017). They also do not monitor elevational gradients as high in elevation or across as many diverse habitat types that I have covered. Additionally, 32
Figure 10: Differences in mammalian seed disperser community species richness between range hypotheses of Solari et al. (2006) (solid line) and with our range hypotheses (dotted lines). Species above do not include members of the Order Chiroptera and have a mass greater than 100g.
33 arboreal species have been particularly overlooked, since most camera trap surveys focus on animals walking on the forest floor (Gregory et al., 2014). Arboreal species, particularly monkeys, play some of the largest roles in seed dispersal (Harrison et al.,
2013) and the forest canopy houses most of the mammalian and avian diversity within the tropics (Gregory et al., 2014). Also, arboreal camera trap studies, to date, have never been conducted along elevational gradients. Increased understanding of the distribution of animals in the tropics will allow us to understand and protect earth’s most biodiverse ecosystem.
34
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43
CHAPTER 2
SEED SURVIVAL AND GRANIVORE COMMUNITY CHANGES ALONG A 2.9KM
TROPICAL ELEVATIONAL GRADIENT
ABSTRACT Trophic interactions and community changes across environmental gradients form some of the foundations of ecology. A unique seed predation study conducted by Hillyer and Silman (2010) along a 2.5km Amazon-Andes elevational gradient documented an interesting pattern in large (>0.4g) seed survival; with rates being lowest at middle elevations (1500m-2400m), increasing at both lower and higher elevations. Given their mass, these seeds must have been removed by vertebrate granivores but the mechanisms that drive this relationship, remain unknown. In this study, I replicated and extended this seed predation study with three seed species (Zea mays, Iriartea deltoidea, and Ormosia coccinea) and used a novel motion-activated camera design to document granivores that visited the stations. With this, I aimed to (1) document granivore diversity and community turnover across the elevational gradient, (2) see which granivores were responsible for the observed seed survival, and (3) determine the environmental factors that may influence the presence of granivores. I documented 34 taxa of granivores, able to handle a wide range of seeds. Cricetid rats were responsible for 66% of overall seed mortality with rates being highest at 2000m, declining at both upper and lower elevations; despite having a lower detection probability at 2000m. Birds and larger mammals
(>100g) were detected only at lower elevations (≤2000m) where they contributed to the observed seed mortality. These results show that the vertebrate granivore community is responsible for the previously described seed mortality. 44
INTRODUCTION
Trophic interactions are central to plant distributional ecology, demography, community composition, and relative abundances (Holl and Lulow, 1997). Seed survival has long been a focus in community ecology, forming some of the foundations of the field (Connell 1978; Janzen 1969; Gillette 1962). Vertebrate granivores in particular play key roles in forest ecosystems through direct consumption of seeds and through secondary seed dispersal in the form of caching (Steele et al. 1993). Vertebrate granivores encompass a broad range of taxa (Hubbell 1980; Vander Wall et al. 2005) that are found across all terrestrial biomes (Janzen 1969), with the highest biodiversity found in tropical rainforests (Christiani and Galletti 2007; Terborgh et al. 1993). Although seed predation experiments have a long history in tropical forest ecology (Gillette 1962;
Janzen 1970), and have demonstrated large effects on forest regeneration (Galetti et al.
2015; Zambrano et al. 2015), few studies have tied seed consumption to individual taxa, despite knowing that specific granivores may be responsible for most seed mortality
(Silman et al. 2003; Tuck Haugassan et al. 2010).
Environmental gradients have long been used to understand the forces that structure communities and their susceptibility and responses to change (Cowles 1899;
Connell 1963; Whittaker 1956). Elevation gradients, in particular, show large changes in community composition, ecosystem function, and form natural laboratories for understanding species responses to climate change (Colwell et al. 2008; Malhi et al.
2010). Although changes in abiotic factors such as temperature and moisture have been a major focus of studies of community structure along elevational gradients (Whittaker
1952; Malcom et al. 2002; Sanders et al. 2007), biotic interactions can have large effects 45
(e.g. Muñoz and Arroyo 2002) and may be equally important. Because elevational gradients show large changes in species composition (e.g. Jankowski et al. 2012; Rovero et al. 2014), they provide the opportunity to understand ecological relationships among species and test the importance of biotic interactions in community structure and ecosystem function in addition to traditionally studied abiotic effects.
Hillyer and Silman (2010) provide a case study in the importance of elevation gradients on trophic structure and species and ecosystem responses to climate change.
Hillyer and Silman studied 24 species of trees ranging in seed size from small (0.002-
0.33g) to large seeds (0.4-3.2g) and found large changes in seed survival across a 2500m
Andes-to-Amazon gradient. Removal of small seeds was highest in lowland areas and decreased rapidly above 1700m, corresponding to the elevation where ant diversity and abundance abruptly decreases (Webb 2008). Large seeds (≥0.4g) show a striking pattern in survival, with seed predation rates being highest at middle elevations (1500-2400m), decreasing towards both upper and lower elevations. Given their mass, these seeds could only be removed by vertebrate granivores. However, the mechanisms behind what dictates the biotic interactions that led to increased predation at middle elevations is unclear, and seed predators were categorized as “vertebrate” despite knowing that there are large changes in the composition and abundance of mammalian and avian granivores with elevation (Solari et al., 2006; Walker et al., 2006). The result provides an opportunity for looking not only at the composition of the granivore community and taxonomic turnover across the elevational gradient, but also link this to trophic interactions (e.g. seed predation, predator-prey) and productivity.
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Vertebrate functional traits and changes in plant-animal interactions
Ecosystem-level vertebrate seed consumption relies on both individual species functional traits and seed predator biomass (Kuprewicz, 2013), both of which vary across environmental gradients, particularly so in the Andes-Amazon, the longest and highest biodiversity forested environmental gradient on earth (Malhi et al. 2000). Granivores in the tropics have evolved traits to overcome some seed defenses but not others, leading to specialization and ecological trade-offs (Leishman 2001). Large granivorous rodents like squirrels and agoutis have sharp, chisel-like teeth and powerful jaws to crack open thick seed endocarps, but lack the digestive processes to properly break down toxic chemicals produced by some seeds (Guimarães et al. 2003). Avian granivory is often overlooked in the tropics (Christiani and Galletti 2007), despite the fact that many bird species have high biomasses (Terborgh 1983; Terborgh et al. 1990), and can break down chemically defended seeds in their crops, if the seeds are small enough to swallow (Rios et al. 2012).
Peccaries have been shown to handle a wide range of seeds including those with chemical defenses and particularly hard endocarps (Kiltie and Terborgh 1983; Kuprewicz 2013;
Silman et al. 2003) but tend not to feed on the smallest of seeds. The most diverse granivores along the elevational gradient are members of Cricetidae with 53 species of rat
(Solari et al., 2010). Although rats preferentially remove small seeds, that have low handling time, if given the chance larger rats will cache larger seeds, although this greatly increases their handling time which can leave them vulnerable to predation (Paiva
Camilo-Alves and de Miranda Mourao 2010).
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Camera Traps: Novel approach to documenting seed mortality
Documenting animal relative abundances is labor intensive and often specializes in only one part of the community (e.g. small mammal live trapping or playback recordings for birds). To alleviate this, specially-placed motion-activated camera traps can be used to document the entire terrestrial community at a site, including small mammals and birds that are often overlooked in traditional camera trap surveys (Lazenby et al. 2015; O’Brien and Kinnaird 2010). One drawback to camera trapping is that species remain “unmarked” and the same individual maybe encountered multiple times, frustrating efforts to assign absolute, and perhaps relative abundances.
An alternative to relative abundance indices is occupancy modeling which can be used to determine a species’ presence or absence at a site (Mackenzie et al. 2002; Royle and Nichols 2003). Occupancy modeling has two important components; site occupancy probability (ψi, the likelihood of a species to occur at sitei) and detection probability (рi, the likelihood that a species is present at a site during a sampling period-p; Ahumada et al. 2013; Mackenzie et al. 2002; Royle and Nichols 2003; Tobler et al. 2015). One advantage of occupancy models is that they take into account imperfect detection of a species at a site or during a sampling period; leading to an estimate always less than 1
(Mackenzie et al. 2002; Murphy et al. 2017). Absences could mean that a species is completely absent from a site or that it is not detected during the sampling period.
Occupancy models also can use predictors (environmental or anthropogenic) that may influence the presence or absence of a species (Lazenby et al. 2015; Niedballa et al. 2015;
Rovero et al. 2014; Tobler et al. 2015). 48
Here I use a well-characterized, high diversity forested Andes-to-Amazon elevational gradient with a well-documented pattern of seed predation/trophic interaction to test hypotheses about the observed seed mortality. In particular, I re-establish the seed choice experiment of Hillyer and Silman (2010) at five elevations and installed a novel camera orientation to document potential granivores and seed removal. Through these seed choice experiments, I aimed to (1) identify the granivore community across the elevational gradient, (2) see how different types of granivores influence seed survival, and (3) through the use of occupancy models, examine what site-specific factors may influence the occupancy of these granivores.
METHODS
Study Site:
The study site is situated in the Kosñipata Valley within Manu National Park,
Earth’s most biodiverse protected area (13° 06’S, 71° 36’E) (Piana and Luna 2016). The site in Kosñipata Valley contains 14 1 ha forest inventory and ecosystem monitoring plots along a 3200m elevation gradient that were installed by The Andes Biodiversity and
Ecosystem Research Group (ABERG) in 2003 (Hillyer and Silman 2010; Malhi et al.
2010; Rapp and Silman 2012). The elevational gradient runs through several different habitats including tropical lowland rainforest (<500m), sub-montane forest (500-1500m), lower montane cloud forest (1500-2400m), upper montane cloud forest (2400-3400m), and the tree line/ puna grassland interface (>3400m) (Malhi et al. 2010). Precipitation levels change greatly along the gradient from as high as 7 meters at 800 meters in elevation to as low as 2.5 meters at 3500 meters in elevation (Rapp and Silman 2012).
Temperature ranges as high as 34°C at 200m to freezing at tree line (Rapp and Silman 49
2012). The advantages of working at this site include a variety of different habitats, a wealth of climatological information, and an expansive knowledge of the local plant communities and ecosystems (Malhi et al. 2010).
Study Species
Animals. The most widespread group of granivores across the experimental site are rats in the family Cricetidae; representing 53 species belonging to 13 Genera within Manu
National Park (Solari et al. 2006). This highly diverse family is present along the length of the gradient, although there is high turnover in species composition with increasing elevation (Figure 1). Larger bodied granivores (mass >100g) at our sites include white- lipped peccary (Tayussa pecari; 25-40kg), collared peccary (Pecari tajacu; 16-27kg), brown agouti (Dasyprocta punctata; 3-4.2kg), spiny rats (Proechimys sp.; 410-1000g), squirrels (Sciurus sp.; 400-600g), lowland paca (Cuniculus paca; 6-12kg), and mountain paca (Cuniculus taczanowskii; 6-10kg). These larger taxa have been the basis of several seed predation studies in the tropical lowland rainforest of Manu National Park (Kiltie and Terborgh 1983; Silman et al. 2003) but 90% of the taxa were restricted to lower elevations (below 1200m; Figure 1; Solari et al. 2006).
Granivorous birds are highly diverse within the study site and are also found at every elevation, with diversity being consistently high until 2000m and decreasing above
(Figure 1). Ground-dwelling granivorous species found at the sites include members of
Tinamidae (tinamous, N=8; 220-1100g), Odontophoridae (wood-quail, N=3; 325-415g),
Cracidae (guans and curassows, N=5; 840-3860g), and Columbidae (oves and pigeons,
N=6; 155-760g) (Walker et al. 2006; Neotropical Birds 2017). Ground-feeding granivores may include members of Corvidae (jays; N=3; 170-312g), Momotidae 50
Figure 1: Species richness of the three major granivore guilds across the elevational gradient. Best fit lines are fit for each type of granivore.
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(motmots; N=4; 170-230g), Thraupidae (tanagers; N=67; 30-120g), Cardinalidae
(cardinals and grosbeaks; N=23; 30-80g), and Emberizidae (sparrows and finches; N=27;
25-112g) (Walker et al. 2006; Neotropical Birds 2017). Although birds have high rates of species turn over across the elevational gradient (Jankowski et al. 2012), most families have at least one member at each elevational site.
Plants. The large C4 grass, Zea mays (Poaceae), the palm, Iriartea deltoidea (Arecaceae), and the canopy tree, Ormosia coccinea (Fabaceae) were used for all seed choice experiments. These seeds had previously been examined by Hillyer and Silman (2010) and have a mass greater than 0.4g so they can only be removed from a site by vertebrate granivores. Zea is a tropical grass that is eaten by a wide range of animals and for the purposes of my experiment, was treated as a non-defended seed. Iriartea is a large palm nut (3.26g±0.62) that is considered a dominant species in the lowland tropical rainforest
(Silman, et al., 2003). Its large size and exceptionally hard endosperm may make it difficult for smaller seed predators to properly consume or remove the seed (Kiltie and
Terborgh, 1983; Kuprewicz, 2012). Members of the Genus Ormosia contain quinolizidine alkaloids which irritate the digestive tracts of many vertebrates and can be lethal in large doses, especially to rodents (Kinghorn et al., 1988).
Camera Design and Seed Arrays:
The seed array experiments were performed during the dry season (May-August) of 2017. For the purposes of this experiment, a site is considered an elevation along the gradient where the cameras were installed (N=9) and a station refers to a dual camera camera array (Figure 2). Of these nine sites, I chose five sites to conduct seed choice experiments (500m, 1500m, 2000m, 3000m, and 3400m) because they were not only 52
Figure 2. A schematic of the camera and seed array set-up showing dual camera setup at each of the seed stations. Picture a) is the view from Camera 1 picture b) is the view from
Camera 2.
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sites of important patterns in seed predation (Hillyer and Silman, 2010) but also where
major shifts in the animal community occur (Solari et al., 2006; Walker et al., 2006), with
4 of 5 sites corresponding to sampling sites used in previous studies of seed predation
along the gradient (Hillyer and Silman, 2010). Four additional camera sites were installed
at 800m, 1750m, 2400m, and 3200m to document transitions in the seed predator
community along the gradient. Within each of the five seed choice experiment sites,
seven camera stations were installed, six of which monitored seed arrays. A seventh
station, without seeds, was also installed in a random location within the site but away
from the other stations to document non-baited detection. A total of 78 cameras were
deployed in the study, resulting in 9,254 camera-days.
Each seed station was installed an average distance from the trail of 28.5m±16.6
and average distance between stations of 33.0m±10.3 (Figure 3). The area these cameras
cover at each site corresponds to 18-34 territories of Cricetid rats (0.16-.29ha; Eubanks et
al. 2011), 2-3 tinamou territories (0.5-1.2ha; Garitano-Zavala et al. 2013), and 1-2 agouti
territories (1-2ha; Aliaga-Rossell et al. 2008). Camera 1 was placed ~1 meter off the
ground, perpendicular to the tree. Camera 2 was placed 0.5 meters at a 45° angle, facing
the seed array to document what granivores removed which seeds. Seeds were placed ~60
cm from the base of the tree and in view of the second camera. Twenty-five Zea were
placed at each station (N=750 in total) from May 15th through May 31st. Twelve Iriartea
were then placed at each station (N=360 in total) from June 8th-June 13th. Five Ormosia
were the last seeds to be placed at each of the stations (N=150 in total) from June 27th-July 3rd. Bushnell MP Trophy Cameras with standard, no-glow, and low glow infrared illumination were randomly assigned to each station. At each station, a 54
Figure 3. A schematic of the camera stations at each seed site. Each station was composed of a dual camera setup.
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12.7cm x 5.7 cm plastic marker was placed in view of the second camera as a size reference to better identify small mammals and birds. Camera stations were checked every 12 days to ensure proper camera function and to census seeds.
Analysis
Photographs of birds and medium-sized granivorous mammals were identified to the species level based on images on the open-access wildlife photography site, ARKive
(Arkive.org, 2016). Smaller rodents, members of Cricetidae and Echimyidae, were identified down to genus based on photographs and measurements taken from preserved specimens at the Smithsonian Museum of Natural History, USA. Based on these photographs and on data collected from NSF-funded trapping campaigns in Manu
National Park (Solari et al., 2006), I am confident in genus-level identifications for all rodents. Photographed species richness of granivores was compared to the actual community as observed by Walker et al. (2006), Solari et al. (2006) and my own observations (Appendix I) to see what percent of the granivore community was captured.
Naïve occupancy (ψ) was calculated by the proportion of stations which had at least one detection of any given granivore (N=39).
Seed survival was analyzed using Cox Proportional Hazard Models (CPHM)
(Cox, 1972). CPHM is one of the many classes of survival models in which individuals are exposed to a risk and the time-to-failure (in this case seed predation) is used to model the hazard rate (Muenchow, 1986). An advantage to this survival model is that covariates can be examined to see if they have an effect on seed survival (Velho et al., 2012;
Kuprewicz, 2013). A crucial covariate, central to both mine and Hillyer and Silman’s study, is elevation and as seed mortality had a unimodal relationship I included a second- 56 order term for elevation in the model. The type of predator that removed a seed was also examined to see if there was an effect of not only all predators (main effect) but individual predator taxa on the survival of seed species. The time of day the hazard occurred was also examined to see if there was a difference between nocturnal predation
(which would have most likely been caused by small rodents) and diurnal predation
(most likely caused by birds and agoutis). Kaplan-Meir Curves were created to show survival over time of each species at each elevation. All analyses were run in R 3.3.1 (R development group, 2016) and used the packages survival and survMisc.
I created occupancy matrices based on the presence and absence of each granivore taxa observed removing seeds. I found that each day (N=68) was acceptable as the unit for the sampling survey for the granivores. I ran single-season occupancy models for each of the granivore species, with and without covariates, using the R software package unmarked. Single-season occupancy modeling was ideal as the survey supported the four major assumptions of this model; (1) detection probability of the species is less than 1 and greater than 0, (2) population at a site is closed during the sampling period, (3) the stations are independent of one another, and (4) differences in detection probabilities of a species within a site can be explained by environmental covariates.
The single season occupancy model allows for site covariates to be tested to explain patterns in either occupancy or detection probability. Central to my objectives, elevation was a crucial covariate that I tested to see what effect it had on occupancy of granivores along the gradient. Elevation was gathered in the field using a Garmin
GPSMap 60CSx unit and then verified in Google Earth Pro. Covariates tested to explain differences in occupancy and detection probabilities of granivores among stations within 57 a site and between sites, I collected data on slope (°) and aspect (compass degrees) using
ArcGIS 10.1. Areas with steeper slope may be avoided by larger mammalian and avian granivores due to restricted movement, thus allowing smaller rodents like Cricetidae and
Echimyidae to more readily occupy the stations (Birn-Jeffery and Higham, 2014). Aspect is the measurement of the direction of an area’s slope that may influence the amount of sunlight a station receives. To convert them from the circular values produced by ArcGIS to linear values, I cosine transformed the aspect values to gain northness and sine transformed the aspect values to gain eastness (Roberts, 1986). Despite not being incorporated in any known occupancy models, I expected occupancy of granivores will be highest on eastern facing slopes where more sunlight reaches the forests, thus allowing for higher primary productivity. Two additional station variables, seeds (coded as 1 or 0 for presence or absence) and habitat (coded as 1-5 based on the 5 previously mentioned habitats), were also examined. Although habitat type was usually homogenous per elevation, the 3400m site had two different habitats (tree line coded as 5 and upper montane cloud forest coded as 4) that may play a role in affecting the species composition and occupancy at this elevation. I used Akaike’s Information Criterion
(AIC) to rank models and models were considered competing if their ΔAIC was ≤ to two.
Detection probability plots were created in R with the packages ggplot2 and popbio.
RESULTS
Seed Predator Community and Diversity
The camera trap survey resulted in 5,104 camera trap days and 7,835photographs of granivores from 34 taxa across the elevational gradient (Figure 4). This represents 49% of the entire terrestrial foraging granivore community being detected in the survey 58
Figure 4: The number of detections for each of the 34 granivores detected during the course of the survey. Taxa are grouped phylogenetically and within taxa, arranged by increasing body size.
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(62% of the mammalian granivore community and 42% of the terrestrial the avian granivore community). The composition of the granivore community varied widely across the elevational gradient (Figure 5) and with a high level of species turnover.
Granivore species richness was highest at 500m (N=20) and declined with increasing elevation, with the sharpest decline at 2000m (Figure 5). The most diverse and prevalent group of granivores along the elevational gradient were members of Cricetidae (N=9;
Figure 5). Larger mammals in the families Cavimorpha, Didelphidae, Sciuridae, and
Tayassuidae had higher diversity from 500m to 1500m declining to only one taxa
(mountain paca, Cuniculus taczanowskii) at tree line (Figure 5). Avian granivore diversity was highest at 500m (N=11) and declined only slightly at 1500m (N=9), although there was high species turnover between these two elevations (Figure 5).
Although there are avian granivores still present above 2000m (Figure 1: Appendix 1), no granivorous birds were detected above 2000m during the seed array experiments (Figure
5).
Seed Survival
Overall seed removal was highest at 1500m and when decomposed into taxa several patterns emerge (Figure 6). This peak at 1500m was due to differential seed predation by granivores within the community at this elevation; avian, Cricetid, and other mammal granivores. Avian granivory peaks at 1500m and is unimportant above this elevation (Figure 6). Larger granivorous mammals (Echimydae, Didelphidae,
Dasyproctidae, and Tayassuidae) removed a near equal proportion of seeds at 500m and
1500m and then don’t play a role above (Figure 6). Cricetid rats were the major granivores across the elevational gradient (Figure 6) and removed the most seeds at 60
Figure 5: The 34 taxa of granivores detected during the course of the survey with their observed elevational distributions broken into three main guilds-Cricetid rats (blue), other mammals (red), and birds (green). Vertical lines show minimum and maximum elevational ranges and the points represent taxa central tendancies. Horizontal dotted lines are placed at seed sites. Taxa are grouped phylogenetically and within taxa, arranged by increasing body size. 61
Figure 6: Proportion of all seeds and their fate at each of the seed choice experimental sites. Seeds either survived the experiment, removed by unknown granivores, removed by avian granivores (Tinamidae, Columbidae, or Motmotidae), removed by other mammal granivores (Dasyproctidae, Echimyidae, Tayassuidae, or Didelphidae), or were removed by Cricetd rats.
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2000m. The proportion of seeds removed by unknown predators had a slight increase at
3000m and 3400m, most likely due to predation by Cricetid rats, which may be undetected given their smaller size (Figure 6). When broken down into individual taxa,
53% (18/34) of granivores actually removed seeds and were highly selective (Figure 7); with the exception of Nephelomys sp. which was able to handle all three seed species.
Seed survival varied across species and across the elevational gradient with patterns similar to those found in previous studies (Hillyer and Silman 2010: Figure 8:
Table 1). Of the 1,260 seeds in the study, 1,002 seeds were removed by granivores; representing a 20% survival of all species across the elevational gradient. Zea had the lowest survival of all seeds, 0% survival across the gradient, which was similar to Hillyer and Silman’s 3% survival (Figure 8a). Predators did not vary in their attack rate of Zea with elevation (χ2 =1.26, df=1, p=0.26; Figure 8a) but they did vary in the time of day the attack occurred (night: χ2 =47.8, df=2, p<0.01 and day: χ2 =47.8, df=2, p<0.01; Table II).
Although predator (main effect) was a significant predictor for seed survival (χ2 =13.05, df=5, p=0.001), individual granivores also played a role in the survival of Zea. Cricetid rats were the major predator of Zea (Figure 7) and their movements were in response to elevation and their nocturnal activity (χ2 =48.76, df=3, p<0.01). Tinamous (χ2 =48.6, df=2, p<0.001) and pigeons (χ2 =36.3, df=2, p<0.001) both had a significant effect on Zea survival (Figure 7), although this was restricted to lower elevations (Figure 6). A small yet significant effect by brown four-eyed opossum (Metachirus nudicaudatus) (χ2 =46.8, df=2, p<0.01) was also documented. Zea was consumed rapidly with 100% mortality across the elevational gradient within 8 days of exposure (Figure 9a). 63
Figure 7: The eighteen granivore taxa that were identified removing seeds across the elevational gradient and the proportion of each seed species the granivore removed. Taxa are grouped phylogenetically and within taxa, arranged by increasing body size.
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at each each at
in this survey (blue line) as compared to the the to compared (blue as line) this in survey
Ormosiasp.
nts are fit with a nonparametric regression using locally weighted locally using regression nonparametric a with fit are nts , and (c) and ,
Iriartea deltoidea Iriartea
(b) (b)
Zea mays, mays, Zea
Survival of (a) of Survival
Figure 8: Figure survival seen byHillyer and Silman, 2010line). (red Points the average are percent of surviving individuals of specieseach elevationand error bars represent95% confidenceintervals. Poi scatterplotsmoothing. 65
Table I: Results of Cox proportional hazard models on seed mortality for each covariate.
Species Covariate 95% Wald P Hazard Ratio Confidence Value Intervals
Zea mays Elevation 0.9999-1.0 0.001 1.002
Predator (Main effect) 0.9663-1.0 0.495 1.019
Predator (Cricetidae) 0.698-1.076 0.122 0.866
Predator (Tinamidae) 0.444-0.793 0.001 0.596
Predator (Columbidae) 0.637-1.136 0.273 0.851
Predator (Didelphidae) 1.0277-9.970 0.046 3.192
Predator (Unknown) 0.698-1.076 0.103 0.823
Time (Main Effect) 0.576-0.8506 0.001 0.704
Time (Night) 1.286-2.375 0.001 1.746
Time (Day) 0.481-1.017 0.000 0.83
Iriartea deltoidea Elevation 0.999-0.999 0.011 0.999
Predator (Main Effect) 1.360-1.561 0.000 1.463
Predator (Cricetidae) 6.044-11.752 0.000 8.428
Predator (Tinamidae) 1.256-12.531 0.019 3.966
Predator (Dasyproctidae) 1.114-2.681 0.015 1.728
Predator (Echimyidae) 1.212-4.680 0.012 2.381
Predator (Unknown) 2.307-4.342 0.000 3.165
Time (Main Effect) 3.2-4.71 0.000 3.882 66
Time (Night) 16.954-41.237 0.000 26.4442
Time (Day) 1.278-2.901 0.002 1.925
Ormosia coccinea Elevation 0.999-0.999 0.0008 0.999
Predator (Main Effect) 1.667-2.246 0.000 1.934
Predator (Cricetidae) 7.078-22.942 0.000 12.733
Predator (Tayassuidae) 0.648-10.983 0.1744 2.667
Predator (Motmotidae) 1.468-6.149 0.002 3.013
Predator (Unknown) 3.087-9.648 0.000 5.457
Time (Main Effect) 2.474-4.913 0.000 3.551
Time (Day) 15.744-63.061 0.000 31.509
Time (Night) 1.606-5.755 0.000 3.040
Table II: Most significant Cox Proportional Hazard Models based on global chi-square test.
Species Covariate DF χ2 P
Zea mays Predator (Main Effect) 1 11.3 0.001
Elevation, Predator (Cricetidae) and Time of Event 2 48.79 0.000 (Night) Interaction
Elevation, Predator (Tinamidae) and Time of Event (Day) 2 48.6 0.000 Interaction
Elevation, Predator (Columbidae) and Time of Event 2 36.3 0.000 (Day) Interaction
Time of Event (Night) 1 21.30 0.000
Time of Event (Day) 1 46.40 0.000
Elevation and Time of Event (Night) Interaction 2 25.70 0.000
Elevation and Time of Event (Day) Interaction 2 47.80 0.000
Iriartea deltoidea Predator (Main Effect) 5 57.40 0.000
Predator (Cricetidae) 3 51.35 0.01
Predator (Tinamidae) 1 39.20 0.000
Predator (Dasyproctidae) 1 39.20 0.000
Predator (Echimyidae) 1 12.50 0.000
Predator (Unknown) 1 21.30 0.000
Time (Main Effect) 1 20.00 0.000
Time (Night) 1 28.90 0.000 67
Predator (Dasyproctidae) and Time of Event (Day) 2 30.70 0.000 Interaction
Predator (Echimyidae) and Time of Event (Night) 2 44.90 0.000 Interaction
Predator (Unknown) and Time of Event (Night) 2 35.30 0.000 Interaction
Ormosia coccinea Predator (Main Effect) 2 15.40 0.000
Predator (Cricetidae) 1 11.47 0.05
Predator (Motmotidae) 1 8.17 0.004
Predator (Unknown) 1 7.61 0.006
Time (Main Effect) 1 10.00 0.002
Elevation 4 2.7 0.05
Time (Night) 1 18.2 0.000
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Figure 9: Average survival of (a) Zea mays, (b) Iriartea deltoidea, and (c) Ormosia coccinea over 54 days at each elevation.
Iriartea survival rates were lowest at middle elevations, increasing towards both
upper and lower elevations (χ2 =0.985, df=1, p=0.01; Figure 8b). Both elevation along
with the time of day an attack occurred (χ2 =20.34, df=2, p<0.01) had significant effects
on seed survival. Seed survival and the effect of elevation, time of attack, and predator
(main effect) had a significant relationship (χ2 =51.35, df=3, p<0.01). Four taxa of
Cricetid rats were the major granivores of Iriartea (Figure 6; χ2 =31.42, df=1, p<0.01).
Diurnal predators like agoutis (Dasyproctidae) and tinamous (Tinamidae) did have a
significant effect on Iriartea (χ2 =38.40, df=2, p<0.001 and χ2 =35.61, df=2, p<0.001,
respectively); despite handling a lower proportion of seeds. Proechimys predation also
had a significant effect (χ2 =7.97, df=2, p<0.019), despite only removing 10 Iriartea
seeds at 500m (Figure 7). Iriartea was discovered quickly at each site (Figure 9b) and,
with the exception of seeds at the 1500m site, granivores stopped removing seeds after 32
days. 69
Ormosia had the highest rate of survival of all three seed species with 67% surviving through the experiment with survival rates being the lowest at 1500m and
2000m, increasing towards both higher and lower elevations (χ2 =2.7, df=4, p=0.05; Figure
8c). Nephelomys sp. was the major predator of Ormosia (Figure 7; χ2 =11.47, df=1, p=0.05). Both predation by collared peccaries (Pecari tajacu) and Rufous Motmot
(Barypthengus martii) had a significant effect on Ormosia survival (χ2 =18.28, df=2, p<0.001 and χ2 =18.29, df=2, p<0.001) despite removing fewer seeds (three and nine seeds, respectively; Figure 7). Ormosia was only removed rapidly at 1500m and 2000m, having minimal mortality at 3000m and 3400m (Figure 9c)
Occupancy of Granivores
Occupancy and detection probabilities of granivore taxa varied widely between
taxa, with taxa that caused most of the witnessed seed mortality having the highest
detection probabilities (Figure 10; Table III). Elevation was an important component of
95% of occupancy models (Table IV), and played a well-observed role in the detection
probabilities of granivore taxa. Detection probabilities for both larger mammalian
granivores and avian granivores followed observed roles in seed survival; detection
probabilities being highest at 500m and 1500m (Figure 11b-c). In contrast, Cricetid rats
had a general increase in detection probability with increasing elevation with highest
detection probabilities at 1500m and 3000m, decreasing slightly at both 2000m and
3400m (Figure 11a). Although seed removal by Cricetids was highest at 2000m, the
detection probability of Cricetids was less than 50% for most of the stations (Figure 11a). 70
Station covariates beyond elevation also played a large role on the detection probabilities of the granivore guilds. Slope had a large effect on the detection probabilities of granivores with the highest probabilities for all granivores below slope of
15.34°; although Cricetid rats still have high detection probabilities at slopes ≥15.34°
(Figure 12). There was no observed preference in aspect for either birds or larger mammals (Figure 13). Cricetid detection probability was highest on eastward facing slopes (13a) but there was no seen relationship with northward facing slopes for any of the taxa (Figure 13b). Habitat type corresponded very closely with elevation for avian and larger mammalian granivores, being restricted to the lowland rainforest and submontane habitats (Figure 14b-c). Cricetid rats had highest detection probabilities in submontane forest and tree-line habitats (Figure 14c). 71
t to largest. Each point represents the average detection probability perdetection probability average the Each point represents to t largest.
baited stations (red) across the elevational gradient. Taxa are ordered phylogenetically and and phylogenetically ordered are Taxa the stations gradient. baited elevational across (red)
-
. Detection probabilities of the 18 granivores that were documented consuming seeds baited at stations documented consuming were that probabilities . granivores 18 the of Detection
Figure 10 Figure non and (black) from smalles withintaxa arranged binomial confidence intervals. site. are bars Error elevational
72
Table III: Granivore naïve occupancy (ψ), estimated occupancy (ψ) and detection probabilities (р) over the entire elevational gradient.
Family Common Scientific Name Naïve ψ SE(ψ) р SE(р) Name Occupancy (ψ)
Columbidae Gray-fronted Leptotila rufaxilla 0.205 0.205 0.065 0.283 0.020 Dove
Cricetidae Akodont Akodon sp. 0.462 0.462 0.079 0.231 0.012
Rice Rat Euryoryzomys sp. 0.128 0.129 0.054 0.069 0.014
Spiny Mouse Neacomys sp. 0.180 0.180 0.0615 0.206 0.019
Rice Rat Nephelomys sp. 0.410 0.41 0.079 0.256 0.013
Arboreal Rice Oecomys sp. 0.077 0.077 0.043 0.096 0.021 Rat
Pygmy Rice Oligoryzomys sp. 0.769 0.769 0.068 0.155 0.008 Rat
Climbing Rhipidomys sp. 0.128 0.128 0.054 0.094 0.016 Mouse
Field Mouse Thomasomys sp. 0.462 0.461 0.080 0.162 0.011
Dasyproctidae Brown Agouti Dasyprocta 0.1026 0.1026 0.0486 0.1250 0.0204 punctate
Didelphidae Brown Four- Metachirus 0.333 0.333 0.076 0.104 0.0104 eye Opossum nudicaudatus
Echimyidae Spiny Rat Proechimys sp. 0.1282 0.1282 0.0535 0.1606 0.0202
Motmotidae Rufous Baryphthengus 0.076 0.075 0.001 0.012 0.007 Motmot martii
Tayassuidae Collared Pecari tajacu 0.051 0.030 0.001 0.002 0.001 Peccary
Tinamidae Black-capped Crypturellus 0.180 0.180 0.061 0.091 0.013 Tinamou atrocapillus
Brown Crypturellus 0.436 0.436 0.079 0.152 0.132 Tinamou obsoletus
Little Tinamou Crypturellus soui 0.231 0.234 0.068 0.063 0.010
Black Tinamus osgoodi 0.202 0.202 0.071 0.0327 0.001 Tinamou
73
across the elevational acrosselevational the
seen seeds seen removing
c) birds c)
ties of a) Cricetid rats, b) other mammals, and mammals, rats, other b) Cricetid a) of ties
Detection probabili Detection
. .
Points are fit with a nonparametric regression using locally weighted scatterplot smoothing. weighted scatterplot locally regression with fit Pointsusing nonparametric a are
nt. nt.
Figure 11 Figure gradie 74
Table IV: Best models for granivore occupancy (ψ) and their corresponding AIC and
ΔAIC values. Covariates include elevation (Elev), seeds (Sds), habitat (Hab), slope
(Slop), north (N), east (E), and aspect (Asp).
Family Scientific Name Model AIC ΔAIC
Columbidae Leptotilla rufaxilla Ψ(Hab+Slop+Sds+E) p(Hab) 535.5 0
Cricetidae Akodon sp. Ψ(Elev+Sds+Hab+Slop) 1148.97 0.0 p(Elev+Sds+Slop)
Ψ(Elev+Sds+Hab+Slop) p(Elev) 1149.09 0.12
Ψ(Elev+Sds+Hab+Slop) 1150.41 1.44 p(Elev+Hab)
Euryoryzomys sp. Ψ(Elev+Hab) p(.) 184.5 0
Ψ(Elev) p(Elev+Sds) 185 0.05
Ψ(Elev+Hab) p(Elev) 185.49 0.99
Neacomys sp. Ψ(Sds+Hab+Slop+N) p(Elev) 427.78 0
Nephelomys sp. Ψ(Elev+Sds+Hab+Slop) 1176.42 0 p(Elev+Hab)
Ψ(Elev+Sds+Hab+Slop) 1178.42 2 p(Elev+Hab+Sds)
Oecomys sp. Ψ(Hab+Sds+Slop) p(.) 134.45 0
Oligoryzomys sp. Ψ(Elev+Sds+Hab+Slop) p(Elev) 1749.56 0
Ψ(Elev+Sds+Hab+Slop) 1750.73 1.17 75
p(Elev+Hab)
Ψ(Elev+Sds+Hab+Slop) 1751.33 1.77 p(Elev+Sds+Hab+Slop)
Rhipidomys sp. Ψ(Elev+Sds+Hab+Slop+Asp) 207.21 0 p(Elev)
Ψ(Elev+Sds+Hab) 207.3 0.09 p(Elev+Sds+Hab)
Thomasomys sp. Ψ(Elev+Sds+Hab+Slop) p(Elev) 998.26 0
Ψ(Elev+Sds+Hab) p(Elev+Hab) 998.76 0.5
Ψ(Elev+Sds+Hab) 1000 1.24 p(Elev+Sds+Hab)
Dasyproctidae Dasyprocta punctate Ψ(Slop+Asp) p(.) 214.26 0
Didelphidae Metachirus nudicaudatus Ψ(Sds+Hab+Slop+E) 549.72 0 p(Elev+Hab+Sds+Slop+E)
Family Scientific Name Model AIC ΔAIC
Echimyidae Proechimys sp. Ψ(Elev+Sds+Hab+Slop) p(Elev) 249.56 0
Motmotidae Baryphthengus martii Ψ(Elev+Hab+Asp) 67.48 1.41
Ψ(Elev+Sds) 88.11 1.7
Tayassuidae Pecari tajacu Ψ(Elev)+ p(Hab) 29.88 0.25
Tinamidae Crypturellus atrocapillus Ψ(Hab) p(Hab) 296.76 0
Ψ(Elev) p(Elev) 296.78 0.02
Ψ(Elev+Sds) p(Elev) 297.73 0.97
Crypturellus obsoletus Ψ(Elev+Seeds+Hab) p(Elev+Hab) 918.96 0
Ψ(Elev+Seeds+Hab+Slop) p(Elev) 920.81 1.85
Crypturellus soui Ψ(Elev+Hab+Slop) 300.94 0 p(Elev+Sds+Hab+Slop)
Tinamus osgoodi Ψ(Elev+Hab+Slop) p(.) 162.57 0
Ψ(Seeds+Hab+Slop) p(Elev) 163.6 1.03
76
Table V: Covariate effects on the occupancy of detected granivores within the survey site. A (+) indicates an increase in occupancy with the covariate and a (-) indicates a decrease in occupancy with the covariate. Habitat is broken up into upper montane cloud forest (UMCF), lower montane cloud forest (LMCF), sub-montane rainforest (SMRF), and lowland tropical rainforest (LTRF). Some taxa with broader habitat preferences were listed as montane cloud forest (MCF), lower montane forest (LMF), and total habitats
(TOT). Covariates include elevation (Elev), seeds (Sds), habitat (Hab), slope (Slop), and aspect (Asp; combined northings and eastings).
Family Common Scientific Name Ψ(Elev) Ψ(Sds) Ψ(Hab) Ψ(Slop) Ψ(Asp) Name
Columbidae Gray-fronted Leptotila (-) (+) (+) (-) (-) Dove rufaxilla LTRF
Cricetidae Akodont Akodon sp. (+) (+) (+) (-) (-) UMCF
Rice Rat Euryoryzomys (-) (+) (+) (+) (+) sp. LTRF 77
Spiny Mouse Neacomys sp. (-) (+) (+) (-) (+) LMCF
Rice Rat Nephelomys sp. (-) (+) (+) (-) (+) LMCF
Arboreal Rice Oecomys sp. (-) (-) (+) (+) (-) Rat LTRF
Pygmy Rice Oligoryzomys (+) (+) (-) (+) (+) Rat sp. TOT
Climbing Rhipidomys sp. (-) (-) (+) (-) (+) Mouse LTRF
Field Mouse Thomasomys sp. (+) (+) (-) (-) (-) MCF
Didelphidae Brown Four- Metachirus (-) (+) (+) (+) (-) eyed nudicaudatus SMRF Opossum
Dasyproctidae Brown Agouti Dasyprocta (-) (+) (+) (+) (-) punctate LMCF
Family Common Scientific Name Ψ(Elev) Ψ(Sds) Ψ(Hab) Ψ(Slop) Ψ(Asp) Name
Echimyidae Spiny Rat Proechimys sp. (-) (+) (+) (+) (+)
LTRF
Tayassuidae Collared Pecari tajacu (+) (-) (-) (+) (+) Peccary LTRF
Tinamidae Black-capped Crypturellus (+) (+) (-) (-) (-) Tinamou atrocapillus LTRF
Brown Crypturellus (-) (+) (+) (+) (+) Tinamou obsoletus MCF
Little Crypturellus (-) (-) (+) (+) (-) Tinamou soui LTRF
Black Tinamus (-) (+) (+) (-) (+) Tinamou osgoodi SMRF
78
79
Figure 12. Detection probabilities of the three major guilds of vertebrate granivores across varying slope degrees. Points are fit with a nonparametric regression using locally weighted scatterplot smoothing.
80
Figure 13. Detection probabilities of the three major guilds of vertebrate granivores across a) eastward facing slopes and b) northward facing slopes. Points are fit with a nonparametric regression using locally weighted scatterplot smoothing.
). Points are fit with a with fit Points ). are
Detection probabilities of the three major guilds of vertebrate granivores across lowland rainforest (LRF), rainforest across lowland vertebrate of major granivores guilds probabilities three the of Detection
. .
nonparametric regression using locally weighted scatterplot smoothing. scatterplot weighted locally using regression nonparametric Figure 14 Figure line tree (UMF), forest and (TL(LMF), upper montane montane (SMF), forest lower forest submontane 81
DISCUSSION
Camera trapping documented not only a highly diverse group of granivores but also their actions by documenting seed removal on precise days. The granivore community was highly variable across the gradient with a wide diversity of granivores in the lowland tropical rainforest (N=20) and sub montane rainforest (N=17), declining to only five species at tree-line. Although the granivore community was diverse along the gradient, this diversity was not reflected upon their role on seed survival with only 53% of detected granivore taxa observed removing seeds. Most seed mortality was caused by members of Cricetidae (66% of the witnessed seed mortality), with rates being highest at
2000m. One Cricetid taxa, Nephelomys sp., was responsible for 13.6% of all seed mortality with detection probabilities being highest at 1500m and 2000m (Figure 10); corresponding to the lowest points of seed survival in both past and current studies
(Figure 8). Detection probabilities for avian and larger mammalian granivores was highest in the lowlands and decreased with increasing elevation (Figure 10). However, 82 the detection probabilities for members of Cricetidae increased with increasing elevation, despite having a slight decrease at 2000m (Figure 10). The methods employed here cannot distinguish whether these increases are due to an increase in Cricetid population with increased elevation or increased foraging activity of those rodents.
Granivore Species Richness, Seed Survival and Occupancy across the Elevational
Gradient.
I captured a diverse assemblage of vertebrate granivores with a variety of body sizes, digestive processes, and jaw mechanics but this alone cannot explain all the observed patterns of seed survival. As predicted, the 500m site had the highest granivore diversity (N=20 taxa) but had similar seed survival to the low diversity 3400m site (N=5 taxa) (Figure 7). The 1500m site had a relatively high diversity of the granivores (N=17;
Figure 5), with the community having a sufficiently broad range of body sizes and ways to overcome seed defenses to handle the wide range of seeds, leading to the lowest point of all species seed survival (Figure 6). The less diverse higher elevation communities
(3000m and 3400m) were primarily made up of Cricetid rats that although perfectly able to remove Zea, only removed a few Iriartea and may not be capable consuming toxic
Ormosia leading to the high survival rate (Figure 8). Thus these high elevation communities may be more adept at handling smaller seeds which are more common at these elevations (Hillyer and Silman, 2010).
Seed Survival and Seed Defenses
Seed survival across the elevational gradient had very similar patterns to Hillyer and Silman (2010) with overall survival being lowest at middle elevations, increasing 83 towards both higher and lower elevations. These patterns can be explained by seed defenses as most granivores were highly selective (Figure 7). Zea had no defenses, was the smallest seed used, and was eaten by the largest proportion of granivores (Figure 7), leading to the lowest survival of all seeds both in my survey, 0% survival, and Hillyer and Silman’s survey, 3% survival (Figure 8a). The physically defended Iriartea was also widely consumed by granivores, although at much lower rates than Zea and with similar patterns as witnessed by Hillyer and Silman, with seed removal rates being highest at middle elevations (Figure 8b). This survival pattern is due to granivores at middle elevations (Nephelomys, agouti, and Black Tinamou (Tinamus osgoodi)) being much more capable at handling Iriartea than granivores at both higher elevations and lower elevations (Figure 6). Although high elevation Cricetid rats like Akodon and Thomasomys removed Iriartea, they did so in more modest proportions than Nephelomys (Figure 7), which was more frequently detected at the middle elevations (Figure 15). Large Cricetid rats and Proechimys did remove Iriartea at 500m but not in large numbers (Figure 6).
Ormosia had not only the highest survival (68%) but also the most distinct survival from Hillyer and Silman’s study (Figure 8c). Although Hillyer and Silman reported no overall difference between mortality of chemically defended seeds, I documented not only a higher rate of survival but also a greater restriction of the granivore community that could actually remove Ormosia (N=3 taxa; Figure 7). The major granivore of Ormosia was Nephelomys, removing 21.33% of Ormosia seeds and although traditionally portrayed as toxic to rodents, studies have shown that Ormosia may be cached by large rodents (Guimarães et al., 2003) and even consumed by some larger Cricetid rats (Galletti et al., 20151). The differences in survival between my 84
Ormosia in this study and past ones may be due to population fluctuations in
Nephelomys. In my study, Nephelomys had low detection probabilities at sites >2000m
(p=0.014) but other studies that have live-trapped in the TMCF found that Nephelomys is still fairly common at these higher elevations (Medina et al., 2012). It is unclear whether the genera is harder to camera trap above 2000m or if there is a lower population at higher elevations; either way releasing Ormosia from potential predation. Other granivores able to consume Ormosia included collared peccaries and Rufous Motmots
(Barypthengus martii) which must be able to break down quinolizidine alkaloids.
Occupancy of Granivores and Seed Survival
Cricetid Rats: Cricetid rats were not only the dominant granivore, but also the most widely detected granivore group across the elevational gradient (Figure 5). The detection probability of Cricetid rats was lowest at 500m and increased with increasing elevation, despite having a slight decrease at 2000m (Figure 10). The past focus of many vertebrate granivory studies in the tropics has been on larger vertebrate granivores (Forget, 1993;
Tuck Haugassan et al., 2010; Silman et al., 2003) but many recent papers have shifted their focus to small mammals, mostly due to many forested areas becoming defaunated due to over-hunting and habitat loss (Galetti et al., 20151; Terborgh et al., 2008). These papers have shown that Cricetid rats can become the dominant granivores in the absence of larger granivores like peccaries and agoutis possibly due to a release from both predators and larger competitors that are present in faunally intact forests. However, my sites at 1500m and above have had few anthropogenic changes showing that for higher elevations, rats may be the dominant granivores in faunated montane cloud forests
(Appendix 1). It is important to note that my site at 500m, even though disturbed roughly 85
20 years ago by selective logging, had similar rates of predation by both Cricetid rats and birds which does correspond to previous papers (Christiani and Galletti, 2007) even though there remains a fairly healthy community of larger animals (Appendix 1).
I am hesitant to say that Cricetid populations are larger at higher elevations than at lower elevations for several reasons. The first being the design of my survey since I assume that each detection is independent of the last one due to the population being unmarked. In other words the higher detection probability may be due to the same group of Cricetid rats occurring at a site, repeatedly. This is highly probable as studies have shown that with increasing elevation, productivity decreases (Girardin et al., 2010) which may drive the Cricetids to forage more, allowing them to encounter the cameras more frequently than at lower elevations. However productivity remains high at 1500m
(Girardin et al., 2010) where detection probability of Cricetid rats remains high. Another possibility could be that Cricetids at 500m have higher predation pressure than Cricetids at higher elevations, restricting their movements and lowering their probability of encountering a camera (Emsens et al., 2014; Murphy et al, 2017). This is highly probable as diversity of avian and reptilian predators is higher at lower elevations (Cattenazi et al.,
2013; Walker et al., 2006) and to add further support to this idea, detection probabilities of mammalian predators is also highest at 500m, decreasing with increasing elevation
(Figure 15). Thus predation could be restricting the movement of Cricetid rats and leading to the lower detection probabilities at 500m.
Avian Granivores: Birds are highly under-examined as granivores in tropical seed predation papers. I found that avian granivores (specifically Gray-fronted Dove (Leptotila rufaxilla) and Brown Tinamou, Crypturellus obsoletus) removed large proportions of Zea 86 from the 500m and 1500m sites (Figure 7) and had high detection probabilities at these elevations (Figure 15). Avian granivores have been documented removing seeds from seed stations; even removing more seeds from stations then rodents (Christiani and
Galletti 2007). Hillyer and Silman noted that ants were most likely the major granivores of small seeds but based on the high detection probabilities of many doves and tinamous at lower elevations, avian granivores should also be considered as they prefer smaller seeds (Rios et al. 2012). Thus avian granivores must be considered in granivory studies, particularly with seeds less than 0.5g.
Figure 15: Average detection probability (p) of mammalian predators at each of the seed sites along the elevational gradient. N is the number of predator species detected at each site. Points are fit with nonparametric regression function using locally weighted scatterplot smoothing. Error bars represent 95% confidence intervals.
87
Non-Cricetid Mammalian Granivores. Although many papers have focused on larger mammalian granivores (in particular peccaries, agoutis, and spiny rats) I found these groups played a minimal role on my observed seed survival (Figure 6 and 7) and most likely played a similar role in Hillyer and Silman’s study. All were also detected less frequently than Cricetid and avian granivores in my study (Figure 13) and seemed to specialize in certain types of seeds (Figure 6). With the exception of mountain paca and
Bolivian squirrel (Sciurus ignitus), all seemed to be restricted to 1500m and lower
(Figure 5). Although both paca species had a large number of detections (Figure 4) and have been recorded as a granivore (Ahumada et al., 2013), neither interacted with the seeds. I also did not document the largest granivore in the study area, the white-lipped peccary, whose presence drastically changes seed survival of large palm seeds (Silman et al., 2003) and could alter the results of Iriartea survival at 500m.
Further Studies
To increase accuracy and better understand tree establishment along the gradient, it may be beneficial to track seeds after they are removed from a station. Although I did not track seeds, I did witness dispersal and recovery of Iriartea at three stations; 2 88 stations at 1500m by brown agoutis (Dasyprocta punctata) and 1 station at 500m by spiny rats. Although I treated removal as equal to predation, this can be biased since rats, agoutis, and spiny rats act as secondary dispersers and may be caching these seeds
(Kuprewicz, 2012; Wenny, 2000). However, this is not a direct mutualistic relationship and a review of the literature shows that seed survival of these dispersed seeds is very low with only 2% of Bertholletia excelsa (Tuck Haugaasen, 2010), 2-10% of
Astrocaryium (Hirsch et al., 2010), and 2% of Dipteryx panamensis (Forget, 1992) germinating successfully in papers that have monitored secondary seed dispersal in the tropics. Given these low rates of germination and the witnessed recovery of some of the dispersed seeds, it is highly likely that most of the seeds were consumed by granivores.
Camera traps proved to be useful tools in documenting granivores that visited the stations. However, not all seed predators that visited a site were documented. Some seeds had been removed between animal detections, showing that granivores did visit the site but were un-detected. Although 1,002 seeds were removed through the course of the survey, with 82% of the removals having a documented granivore, 18% are still classified as being taken by an unknown predator (Figure 16a). Of these, 78% of unknown predation occurred at night and was likely due to rats since they were most active at night
(Figure16b). Diurnal seed removals may have been due to doves, tinamous, or agoutis; the first two being the most prevalent diurnal granivores at the lower elevation stations
(Figure 6). Regardless, given the high percentage of successful and reliable documentations of granivores, camera traps offer the ability to tie seed predation to individual taxa and should be used in more seed predation studies.
89
Figure 16: Proportion of all seeds consumed by a) all granivores broken down into four guilds and b) proportion of unknown granivores broken into nocturnal and diurnal granivory.
90
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101
APPENDIX 1: Taxa documented in the 2013 and 2016 surveys in Manu Biosphere
National Park. Families and scientific names are based on those used by The IUCN Red
List. Elevations are recorded in meters with documented photos outside their elevational ranges in bold. Habitats are based on forest structure and include lowland rainforest (LF)
<500m, submontane forest (SM) 500-1500m, lower montane forest (LM), upper montane forest (UM) , tree line (TL), and wet puna (PU). Numbers indicate important notes on taxa or new taxa to the park. Bold lettering represents a novel elevation where a taxa was detected.
Family Scientific Name Common Name Elevations Habitats Recorded in the Recorded Surveys
Didelphidae Didelphis Common Opossum 523m-2180m SM, LM marsupialis
Didelphis pernigra 1 Andean White-eared 1982m-3282m LM, UM Opossum
Gracilianus sp.2 Mouse Opossum 500m-3432m LF, SM, LM, UM, TL
Marmosa sp.2 Mouse Opossum 500m-3432m LF, SM, LM, UM, TL
Marmosops sp.2 Slender Opossum 500m-3432m LF, SM, LM, UM, TL
Metachirus Brown Four-eyed 522m-1521m LF, SM, LM nudicaudatus Opossum
Philander opossum Four-eyed Opossum 548m LF
Chlamyphoridae Priodontes maximus Giant Armadillo 500m-537m LF
Dasypodidae Dasypus kappleri 3 Long-nosed Armadillo 500m-539m LF
Dasypus Nine-banded Armadillo 522m-1266m LF, SM novemcinctus
Myrmecophagidae Myrmecophaga Giant Anteater 500m LRF, SM tridactyla
Tamandua Southern Tamandua 500m-1505m LF, SM, LM tetrodactyla 102
Family Scientific Name Common Name Elevations Habitats Recorded in the Recorded Surveys
Caenolestidae Lestoros inca Incan Shrew 2680m-3325m UM
Leporidae Sylvilagus Tapeti 500m-539m LF brasiliensis
Sciuridae Sciurus ignitus 4 Bolivian Squirrel 1266m-1982m SM, LM
Sciurus igniventris North Amazon Red 1500m SM, LM Squirrel
Sciurus spadiceus Southern Amazon Red 528m LF Squirrel
Cricetidae Akodon sp. 6 Akodont 1898m-3461m LM, UM, TL
Euryoryzomys sp. 7 Cotton or Rice Rat 527m-750m LF, SM
Microryzomys Montane Colilargo 2180m-3282m LM, UM minutus
Neacomys sp. 8 Spiny Mouse 522m-2180m LF, SM, LM
Nectomys apicallis 9 Western Amazonian 522m LF Water Rat
Nephelomys sp. 10 Cotton or Rice Rat 1266m-3440m SM, LM, UM
Oecomys sp. 11 Arboreal Rice Rat 522m-750m LF, SM
Oligoryzomys sp. 12 Pygmy Rice Rat 524m-3461m LF, SM, LM, UM, TL
Oxymycterus sp. 13 Shrew Rat 2900m-3461m UM, TL, PU
Rhipidomys gardneri Gardner’s Long-tailed 500m-1521m LF, SM, LM Rice Rat
Thomasomys sp. 14 Mountain Field Mouse 1988m-3461m LM, UM, TL, PU
Dasyproctidae Dasyprocta Central American Agouti 750m-2200m SM, LM punctata 15
Cuniculidae Cuniculus paca Lowland Paca 500m-1750m LF, SM, LM
Cuniculus Mountain Paca 1898m- 3557m LM, UM, TL, taczanowskii PU
Echimydae Proechimys sp. 16 Spiny Rat 500m-750m LF, SM
Atelidae Lagothrix cana Gray Woolly Monkey 1492m SM
Cebidae Cebus albifrons White-fronted Capuchin 1289m-1492m SM 103
Family Scientific Name Common Name Elevations Habitats Recorded in the Recorded Surveys
Canidae Atelocynus microtis Short-eared Dog 750m SM
Speothos venaticus Bush Dog 3000m UM
Ursidae Tremarctos ornatus Andean Bear 2200m-3562m LM, TL
Procyonidae Nasua nasua South American Coati 750m SM
Nasuella sp. 17 Mountain Coati 1750m-2900m LM, UM
Potos flavus Kinkajou 2102m LM
Mustelidae Eira barbara Tayra 519m-3451m LF, SM, LF, UM, TL
Galictis vittata Greater Grison 1498m SM, LM
Lontra longicaudis Neotropical Otter 527m LF, SM
Mustela frenata Long-tailed Weasel 1988m-3557m LM, UM, TL, PU
Felidae Leopardus pardalis Ocelot 500m-750m LF, SM
Leopardus tigrinus 18 Oncilla 1266m-3461m SM, LM, UM, TL
Leopardus weidii Margay 500m LF
Pathera onca Jaguar 500m-1750m LF, LM
Puma concolor Puma 500m-3170m LF, SM, LM, UM
Puma yagouarundi Jaguarundi 500m-1266m LF, SM
Tapiridae Tapirus terrestris South American Tapir 522m-750m LF, SM
Cervidae Mazama americana South American Brocket 500m-750m LF, SM Deer
Mazama chunyi Peruvian Dwarf Brocket 2200m-3368m LM, UM Deer
Tayassuidae Pecari tajacu Collared Peccary 500m-1500m LF, SM, LM
Tinamidae Crypturellus Black-capped Tinamou 500m-750m LF, SM atrocapillus
Crypturellus cinereus Cinereous Tinamou 500m-538m LF, SM
Crypturellus Brown Tinamou 524m-3096m LF, SM, LM, obsoletus UM 104
Family Scientific Name Common Name Elevations Habitats Recorded in the Recorded Surveys
Crypturellus soui Little Tinamou 522m-1522m LF, SM, LM
Crypturellus Undulated Tinamou 524m-750m LF, SM undulatus
Nothocerus Hooded Tinamou 1476m-3313m SM, LM, UM nigrocapillus
Nothoprocta Taczanowski’s Tinamou 3447m TL, PU taczanowskii
Tinamus major Great Tinamou 750m SM
Tinamous osgoodi Black Tinamou 750m-1520m SM, LM
Tinamus tao Gray Tinamou 750m-1505m SM, LM
Odontophoridae Odontophorus Stripe-faced Wood-Quail 2102m-3096m LM, UM balliviani
Odontophorus Rufous-breasted Wood- 1476m-1521m SM, LM speciosus Quail
Odontophorus Starred Wood-Quail 500m-750m LF, SM stellatus
Cracidae Aburria aburri Wattled Guan 1507m-2200m LM
Mitu tuberosum Razor-billed Curassow 500m-750m LF, SM
Penelope jacquacu Spix’s Guan 522m-750m LF, SM
Accipitridae Buteo sp.19 Hawk 3457m PU
Buteogallus Great Black Hawk 500m LF, SM urubitinga
Rallidae Aramides cajanea Gray-necked Wood-Rail 522m-537m LF, SM
Psophiidae Psophia leucoptera Pale-winged Trumpeter 750m SM
Eurygidae Eurypyga helias Sunbittern 500m LF
Columbidae Geotrygon frenata White-throated Quail- 520m-3042m LF, SM, LM Dove
Geotrygon montana Ruddy Quail-Dove 522m-750m LF, SM
Leptotila rufaxilla Gray-fronted Dove 500m-750m LF, SM
Cuculidae Neomorphus Rufous-vented Ground- 527m-750m LF, SM geoffroyi Cuckoo
Trochilidae Anthracothorax or Hummingbird 522m LF, SM Colibri sp. 20 105
Family Scientific Name Common Name Elevations Habitats Recorded in the Recorded Surveys
Momotidae Barypthengus martii Rufous Motmot 524m-1460m LF, SM
Galbulidae Jacamerops aureus Great Jacamar 528m LF, SM
Picidae Veniliornis nigriceps Bar-bellied Woodpecker 3578m UM, TL
Furnariidae Asthenes sp.21 Canastero sp. 3082m-3096m UM
Campylorhamphus Red-billed Scythebill 522m LF, SM trochilirostris
Cranioleuca Creamy-crested Spinetail 2988m-3034m UM albicapilla
Furnarius leucopus Pale-legged Hornero 500m-538m LF, SM
Margarornis Pearled Treerunner 1522m-2000m LM squamiger
Philydor ochrogaster Ochre-bellied Foliage- 1266m SM gleaner
Synallaxis azarae Azara’s Spinetail 2988-3427m UM, TL
Thripadectes holostictus Striped Treehunter 1532m LM
Xiphorhynchus Olive-backed 1500m LM triangularis Woodcreeper
Thamnophilidae Cercomacra serva Black Antbird 522m-1521m LF, SM, LM
Myrmeciza Black-throated Antbird 528m LF, SM atrothorax
Pyreglena leuconata White-backed Fire-eye 1476m-2032m SM, LM
Taraba major Great Antshrike 534m LF, SM
Formicariidae Chamaeza Short-tailed Antthrush 1266m-1521m SM, LM campanisoma
Chamaeza Barred Antthrush 2200m-2506m LM, UM mollissima
Formicarius analis Black-faced Antthrush 750m SM
Formicarius Rufous-breasted 1492m-1521m SM, LM rufipectus Antthrush
Grallariidae Grallaria albigula White-throated Antpitta 1750m-2200m LM
Grallaria Red and White Antpitta 2022m-2776m LM, UM erythroleuca 106
Family Scientific Name Common Name Elevations Habitats Recorded in the Recorded Surveys
Grallaria Scaled Antpitta 1266m SM guatimalensis
Grallaria rufula Rufous Antpitta 2900m-3461m UM, TL
Grallaria squamigra Undulated Antpitta 3282m-3368m UM
Grallaricula Ochre-breasted Antpitta 3461m UM ferrugineipectus
Grallaricula Ochre-breasted Antpitta 2102m LM flavirostris
Hylopezus berlepschi Amazonian Antpitta 522m-528m LF, SM
Myrmothera Thrush-like Antpitta 527m LF, SM campanisoma
Conopophagidae Conophaga Slaty Gnateater 1500m-1522m SM, LM ardesiaca
Rhinocryptidae Scytalopus atratus White-crowned Tapaculo 1521m-1898m LM
Scytalopus sp. Tapaculo 2900m-3427m LM, UM, TL
Tyrannidae Corythopis torquatus Ringed Antpipit 522m-524m LF, SM
Elaenia sp.22 Elaenia 1986m LM
Ochthoeca frontalis Crowned Chat-Tyrant 3423m-3462m UM, TL, PU
Ochthoeca Rufous-breasted Chat- 3578m TL, PU rufipectoralis Tyrant
Pseudotriccus Rufous-headed Pygmy- 3034m UM ruficeps Tyrant
Pipridae Pipra fasciicauda Band-tailed Manakin 524m LF, SM
Troglodytidae Henicorhina Gray-breasted Wood- 1982m-2386m LM leucophrys Wren
Thryothorus leucotis Buff-breasted Wren 522m LF, SM
Turdidae Catharus fuscater Slaty-backed 1505-3170m SM, LM, UM Nightengale-Thrush
Turdus albicollis White-necked Thrush 538m LF, SM
Turdus fuscater Great Thrush 3038m-3557m UM, TL, PU
Turdus leucops Pale-eyed Thrush 1266m SM
Turdus serranus Glossy-black Thrush 2506m-3461m UM 107
Family Scientific Name Common Name Elevations Habitats Recorded in the Recorded Surveys
Thraupidae Diglossa cyanea Blue Masked Flower 3034m-3368m UM Piercer
Diglossa lafresnayi Moustached Flower 3048m-3461m UM, TL Piercer
Iridosornis analis Yellow-throated Tanager 2022m LM
Emberizidae Arremon Chestnut-capped Brush- 1505m-2200m SM, LM brunneinucha Finch
Arremon taciturnus Pectoral Sparrow 522m-538m LF, SM
Arremon torquatus Stripe-headed Brush- 2000m-3368m, LM, UM Finch
Atlapetes Black-faced Brush-Finch 1898m-3423m LM, UM, TL melanolaemus
Parulidae Basileuterus Citrine Warbler 3050m-3461m UM, TL luteoviridis
Basileuterus signatus Pale-legged Warbler 1505-2000m SM, LM
Myioborus Spectacled Redstart 3000m UM melanocephalus
Myiothlypis Buff-rumped Warbler 527-528m LF, SM fulvicauda
Teiidae Ameiva ameiva Giant Ameiva 538m LF, SM
Tupinambis teguixin Golden Tegu 528m-537m LF, SM
Colubridae Chironius monticulus Mountain Whipsnake 2022m-3082m LM, UM
108
CURRICULUM VITAE Daniel A. Lough
Education: University of South Florida: Tampa, Florida Bachelor of Science Degree (Integrative Animal Biology): December 2014
Wake Forest University: Winston-Salem, North Carolina Master of Science Degree (Ecology): Expected December 2017
Teaching: 2010-2015: Education Instructor. Tampa’s Lowry Park Zoo. 2015: Watershed’s Investigations Instructor. The Florida Aquarium. 2015-2017: Teaching Assistant (Comparative Physiology). Wake Forest University.
Grants: North Carolina Academy of Sciences Bryden Grant (2016) Wake Forest University’s Vecellio Grant (2016) Paul K. and Elizabeth Cook Richter Memorial Fund (2016)