69EG3291 Third Year Project

An Investigation into the Effects of Tourist Related Disturbances on Parrot Abundance and Behaviour at a Peruvian Geophagy Site

S. Lovesey

A project submitted in partial fulfilment of the requirements for the degree of Bachelor of Science (Honours) in Physical Geography, The Manchester Metropolitan University.

Department of Environmental and Geographical Sciences The Manchester Metropolitan University

April 2007

1 Declaration of originality

This is to certify that the work is entirely my own and not of any other person, unless explicitly acknowledged (including citation of published and unpublished sources). The work has not previously been submitted in any form to the Manchester Metropolitan University or to any other institution for assessment or for any other purpose.

Signed ------

Date ------

2 Contents

Contents ii Contents iii List of figures iv List of tables v Abstract vi

1.0 INTRODUCTION 1 1.1 Diversity in the rainforest 1 1.2 Threats to tropical wildlife 1 1.3 Parrots 2 1.3a. Parrot diversity 2 1.3b. Parrot ecology 2 1.3c. Threats to parrots 3 1.3d. Conservation of parrots 4 1.3e. Parrots of Peru 5 1.4 Geophagy 5 1.4a. What is geophagy? 5 1.4b. Geopagy in parrots 5 1.4c. The absorption of dietary toxins and gastrointestinal protection 6 1.5 Parrot abundance and geophagy in southeastern Peru 7 1.6 Ecotourism and parrots in Peru 8 1.7 Effects of tourist visitation on parrot geophagy sites 9

2.0 AIMS 9

3.0 STUDY AREA 10 3.1 Peru 10 3.2 Study site 11 3.3 The La Torre colpa 12 3.4 Tourist visitation 13 4.0 METHODOLOGY 13 4.1 Parrot observations 13 4.2 General disturbances 14 4.3 Tourist disturbances 14 4.4 Boat disturbances 15 4.5 Animal disturbances 15 4.6 Unknown disturbances 15 4.7 Statistical analysis 15 4.7a. Associations 15 4.7b. Variances between disturbance factors 16

5.0 RESULTS 16 5.1 Numbers recorded 16 5.2 Species associations 18

3 5.3 Parrot abundance and days of disturbance 19 5.4 Species associations with different disturbance factors 20 5.5 General disturbance factors 21 5.6 Tourist disturbance factors 22 5.7 Boat disturbance factors 22

6.0 DISCUSSION 23 6.1 Abundance 23 6.1a. Most abundant species 23 6.1b. Least abundant species 24 6.1c. General abundance of species 24 6.2 Species associations 25 6.3 Species interdependence 25 6.4 General disturbance and parrot abundance 25 6.4a. Associations with general disturbance factors 26 6.4b. Differences observed between general disturbance factors 26 6.5 Tourist disturbance factors 27 6.5a. Cough/sneeze and dropped objects 27 6.5b. Loud talking 27 6.5c. Quiet talking 28 6.5d. Arrival and departure 28 6.6 Boat disturbance 29 6.6a. Loud boats not stopping 29 6.6b. Quiet boats not stopping 29 6.6c. Tourist boats stopping 30 6.7 Limitations of the study 30 6.8 Management implications 31 6.8a. Abundance of species 31 6.8b Tourist disturbances 31 6.8c Boat disturbances 32

7.0 CONCLUSION 33

8.0 Acknowledgements 34

9.0 References 34

10.0 Appendices 45 Appendix 1 - Example of data sheet used to record parrot abundances 45 and flushes Appendix 2 - General information about the parrot species 46 recorded at the La Torre colpa

4 List of figures

Figure 1 Map of Peru showing location of study site 10

Figure 2 Satellite image of the Tambopata, La Torre colpa, Inotawa Lodge and 11 Posada Amazonas.

Figure 3 View of the La Torre colpa from the Inatowa Blind. 12

Figure 4 Mean disturbance levels compared to mean parrot visitation numbers 20 per day.

5 List of tables Page

Table 1 Total number of individual birds observed feeding by species/day. 17

Table 2 Mean number of individual birds observed feeding per day. 18

Table 3 Species associations using Spearman’s rank correlation. 19

Table 4 Species/disturbances associations calculated using Spearman’s rank 21 correlation.

Table 5 Mean and standard deviation values comparing general disturbance 21 factors with tree and colpa flushes.

Table 6 Mean and standard deviation values comparing tourist disturbance 22 factors with tree and colpa flushes.

Table 7 Mean and standard deviation values comparing boat disturbance with 23 tree and colpa flushes.

6 Abstract

Geophagy, the intentional consumption of soil or clay, plays a vital role in maintaining parrot health. This research investigates the effects that tourist related disturbances and boat traffic are having on parrots at a geophagy site, situated on the river Tambopata, southeastern Peru. Five minute counts were used to establish parrot abundance with flushes being recorded as signs of disturbance. Impulse noises such as the onset of loud talking, coughing/sneezing and dropped objects resulted in the greatest tourist disturbance to parrots overall. Boats using peke-peke motors attributed the most disturbances by boats to parrots at the site. Simple guidelines on talking levels inside the blind should be put into place. An alternative floor covering should also be used to reduce the impact of dropped objects. Speed limits and passing distances for boats could also be used to reduce disturbance further. Overall the study was successful but further research needs to be undertaken on the actual quantities of clay needed for parrots to remain healthy. Studies similar to this at other parrot geophagy sites would also greatly contribute to the limited knowledge that has already being gained.

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7 1. INTRODUCTION

1.1 Diversity in the rainforest

Tropical rainforests are the most diverse habitat on the planet (Bierregaard et al 1992). Even though they only cover 7% of the planet’s landmass, they are home to half to two thirds of the plant and animal species on Earth (Wilson 1988, Raven 1988). Due to this great diversity of life they have become known as biodiversity hotspots, which are vital when considering the conservation of many tropical species (Mittermeir et al 1998). Pressure on the world’s rainforests is ever increasing due to expanding human populations who require land to live on and provide income (Laurance 2001).

1.2 Threats to tropical wildlife

Globally tropical rainforests are coming under continuing threat from human activities (Turner 1996). Deforestation is the main threat faced by tropical rainforests and wildlife (Geist et al 2002, Putz et al 2000). Logging for the international timber trade, forest conversion for crop cultivation, clear felling for grazing arable land and traditional practises such as agroforestry and swidden farming techniques, all combine to fragment and disturb a rainforest’s natural dynamics and habitats (Sivakumar 2000, Blockhus et al 1992, Bowles et al 1998). It is estimated that over the period 1995- 2000, 1.9 million ha per year of Amazonian rainforest were lost to these activities (Laurance et al 2001).

Habitat loss and conversion are the direct effects of logging on tropical rainforest wildlife, however there are secondary factors to consider. Associated with logging and deforestation is an increase in hunting pressure for food and the bush-meat trade (Sandercock et al 2000). This is due to once inaccessible areas of forest being opened up through road building in order to access and remove timber or crops (Bennet et al 2000, Uhl et al 1989). People will expand along new infrastructure clearing patches of forest for personal home-gardens and subsistence agriculture (Kellman et al 1997, Johns et al 1996). Many will rely on bush meat and trapping to provide extra income, increasing the pressure on wildlife resources in that area (Fa et al 2002, Carpaneto et al 2004).

8 1.3 Parrots

1.3a Parrot diversity

Parrots (of the order Psittaciformes) are one of the largest and uniformly distinctive groups of birds in the world (Juniper & Parr 1998). There are around 353 different species that can be divided into two families (Snyder et al 1996): Cacatuidae (cockatoo) and Psittacidae (true- parrots). Members of the parrot family include macaws, parakeets, and parrotlets (Snyder et al 2000). They can be be found in most warm regions of the world, including India, southeast Asia, the Neotopics and west Africa (Juniper et al 1992). Parrots become increasingly diverse in tropical and subtropical lowland forested areas, with the most speciation occuring in the New World and Australia (Karr 1976).

1.3b. Parrot ecology

Most parrots dwell in forest habitats and are threfore largly or exclusivly arboreal, however there are exceptions, such as the kakapo Strigops habroptilus of New Zealand (Clout et al 1995), and the ground parrot Pezoporus wallicus Kerr of Australia (Meredith et al 1984). Most parrot diets are comprised of plant parts in the form of seeds, fruits, blossoms, nectar, pollen, buds, leaves, berries, nuts and sometimes bark (Juniper & Parr 1998, Galletti 1993). Many are generalist feeders with a wide dietary flexiblity that allows them to spread over large and ecologically diverse ranges, whilst others are specialists associated with a small habitat range and a less varied diet, such as the endangered Lear’s macaw Anodorhynchus leari (Yamashita 1987). The majoritory of species are gregarious for at least part of the year and are usually encountered in small flocks or pairs, attributed to foraging effectivness and anti-predator defence (Monterrubio-Rico et al 2006, Gilardi et al 1988, Burger et al 2003). Social roosting is common in parrots (Chapman et al 1989). Some species like the African grey Psittacus erithacus, spend the night in tree tops (Juniper & Parr 1998), other species in small groups in tree hollows (Pyrrhura parakeets, Best et al 1996), some on cliffs (Brightsmith 2005), or others in communial nests (monk parakeet Myiopsitta monochus, Sol et al 1997). Parrots are mainly monogamous and in the case of many larger species will pair for life (Loffredo et al 1986). The vast

9 majoritory of species are cavity-breeders, with nests located in tree hollows (Bessinger et al 1992, Brightsmith 2005). The availability of suitable nest-sites is a limiting factor in the breeding density of many parrot species due to very few activly constructing nests (Renton et al 1999).

1.3c Threats to parrots

The World Conservation Union (IUCN), has identified two main threats to parrot species, trapping for the live bird trade, and habitat loss and fragmentation (Snyder et al 2000). Due to their attractiveness and intelligence parrots have always been highly desired as pets (Cooney et al 2005). This has led to vast quantities of new world parrots being exported from Third World to First World countries in order supply private buyers and aviculturlists (Guix et al 2004). More than 1.8 million parrots legally entered the international trade from 1982-1988, most imported into the United States (80%), European Union countries (15%) and Japan (3%) (Bessinger et al 1992). Estimates of mortality rates and illegal smuggling indicate that the actual number of birds taken from the wild may be two to three times greater than this figure (Iñigo- Elias et al 1991).

As the international trade in parrots depletes numbers in the wild they also face the effects of habitat destruction and conversion that threatens all wildlife in the tropics (Geist et al 2002, Putz et al 2000, Turner 1996). Research into bird extinctions in tropical rainforests suggests that a 1000 ha area of fragmented rainforest will support only 50 percent of the original bird species recorded before fragmentation occurred (Brooks et al 1999). Every parrot species has its own reaction to forest disturbance according to habitat selection, foraging behaviour, dietary adaptability and sensitivity to microclimatic conditions (Thiollay 1997). Habitat loss and conversion combined with legal and illegal trade has left at least 30% of the 140 parrot species found in the Western Hemisphere now being threatened with extinction (Collar et al 1992). Research suggests that 40% of these species are threatened primarilly by habitat destruction, 17% by trade, 36% by a combination of the two causes and 7% by other factors (Collar et al 1992), making neotropical Psittacidae one of the most threatened groups of birds in the world (Bennet et al 1997). This illustrates the need for continuing research into the many effects that human acivities are having on the

10 world’s parrot species. This can then be used in creating effective management plans to aid in the global conservation in parrots.

1.3d. Conservation of parrots

Conservation efforts to ensure the protection of parrots and other species have been undertaken since the 1960s (Myers et al 2000). The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), is an international agreement between governments (CITES 2007). Its aim is to ensure that international trade in specimens of wild animals and plants does not threaten their survival. Along with the establishment of conventions like CITES, organisations such as the IUCN and BirdLife International campaign and fund for the preservation of parrot species (Jenkins 1996, BirdLife International 2006).

Along with environmental conventions and the activities of other organisations, more general practises are evolving that aid in parrot conservation, due to the growing international concern over the destruction of the world’s tropical rainforests (Smyth et al 2004). Measures are being taken to reduce the levels of deforestation that are currently occurring, and the habitat loss that is associated with it (Bawa et al 1998, Lambert 1992). Practises such as selective logging and supervised logging regimes are increasingly being used to reduce damage to forest habitats that is usually associated with traditional logging regimes (Lewis 2001, Whitman et al 1998, Asner 2004). This involves directional felling to reduce damage done to the remaining stand, liana cutting to avoid destroying the forest canopy, more care in planning roads and skid trails, leaving refuge stands to initiate forest regeneration and not logging on steep slopes to prevent soil erosion (Packer 1967, Burke 1973, Holmesay et al 2002). This reduces the habitat loss and disturbance that occurs through traditional logging practises, and promotes faster forest regeneration times (Torquebiau 1992). This benefits the whole wildlife community that depend on tropical rainforest habitats for survival (Hamer et al 2003, Dah 2004). This however, will only go part of the way to aiding in parrot conservation, as it is far to general. Many species will need independent research into specific management plans to help individual species depending on habitat preference, ecology and abundance.

11 1.3e. Parrots of Peru

Peru has an incredible diversity of bird species, approximatly 1878 species inhabit Peru with 139 of those being endemics (Clements 2001). 52 parrot species have been recorded with one being endemic to the country (yellow-faced parrotlet Forpus xanthops). There are 10 globally threatened species that have been identified on the IUCN’s Red List of Threatened Species (IUCN 2007). These are military macaw Ara militaris (vulnerable), blue-headed macaw Primolius couloni (endangered), red- masked parakeet Aratinga erythrogenys (near threatened), golden-plumed parakeet Leptosittaca branickii (vunerable), white-necked parakeet Pyrrhura albipectus (vulnerable), yellow-faced parrotlet Forpus xanthops (vulnerable), gray-cheeked parakeet Brotogeris pyrrhopterus (endangered), amazonian parrotlet Nannopsittaca dachilleae (near threatened), spot-winged parrotlet Touit stictopera (vulnerable) and red-faced parrot Hapalopsittaca pyrrhops (vulnerable).

1.4 Geophagy

1.4a. What is geophagy?

Geophagy is the intentional consumption of soil or earth (Brightsmith et al 2004). This has been recorded primarily in the tropics amongst many different species. These include mammals (Jones et al 1985, Klause et al 1998), birds (Symes et al 2006, Montenegro 2004), reptiles (Brown 1981) and invertebrates (Wolters 2004). The principle theories as to why this behaviour occurs include mechanical enhancement of digestion, mineral supplementation, acid buffering, the absorption of dietary toxins and gastrointestinal cytoprotection (Gilardi et al 1999, De Souza et al 2002). However, different animals consume clay or soil for different reasons so one hypothesis cannot be true for all species.

1.4b. Geophagy in parrots

Geophagy amongst birds has been described from observations of many species, but is particularly well known to occur in the parrot family. Reports of parrot geophagy in the

12 Neotropics have come from Mexico, Bolivia, Brazil and Peru; however parrot geophagy is not limited to this region. Observations of soil consumption have been recorded in the palm cockatoo Probosciger aterrimus, of Papua New Guinea (Symes et al 2005), and the grey lourie Corythaixoides concolor, in Botswana (Pyrce 2004). As this behaviour is often overlooked, it is expected that new observations in varying species will be made that support the theory that avian geophagy is widespread, and has evolved several times independently (Gilardi et al 1999).

1.4c. The absorption of dietary toxins and gastrointestinal protection

The most extensive data on parrot geophagy comes from Peruvian clay-lick sites (Brightsmith et al 2004, Gilardi et al 1999, Hammer 2002). Studies indicate that there are two main reasons for geophagy in parrot species, the absorption of dietary toxins and gastrointestinal protection (Brightsmith et al 2004, Gilardi et al 1999). Soil samples collected and analysed from several Peruvian clay-lick sites demonstrate that soils consumed have the ability to absorb large quantities of alkaloid quinine (Brightsmith et al 2004). This toxin occurs naturally at low levels in most parrot diets. Soil analysis showed that the clays could absorb ~100 mg of alkaloid quinine per gram of clay consumed. This indicates that the consumption of several grams of clay per day could absorb biologically significant quantities of this toxin, enabling an increase in dietary capability.

The consumption of clay to absorb dietary toxins can also be linked to gastrointestinal protection (Gilardi et al 1999). The presence of clay in the gut increases mucus secretion and enhances the mucus barriers ability to protect the gut lining from chemical attack (Diamond et al 1999). Research into the passage rate of clays in captive parrots indicates that large amounts of clay were still present in the gastrointestinal tract for at least 12 hours after consumption (Gilardi et al 1999). Most parrot species that exhibit geophagy behaviour consume clay daily, with most consumption occurring in the early morning. This can be used as evidence for clay being used for the absorption of dietary toxins and gastrointestinal protection throughout the day as birds feed (Brightsmith et al 2004). The absorption of dietary toxins and gastrointestinal protection benefits clay- consuming parrot species by enabling birds to consume previously unexploitable resources and/or increased quantities of seeds and fruits that would otherwise cause

13 illness or death (Gilardi et al 1999). It also allows birds to consume nutritionally rich but highly toxic resources during the dry season when food is a limiting factor to other frugivores (Terborgh 1986). Therefore, in the case of parrots, geophagy extends their dietary capacity and may increase distributions and abundances of certain of species. This highlights how important geophagy is too many parrot species, which have evolved this behaviour to increase their health and survival rates. Due to this it is vital to understand any effects that human disturbances at parrot geophagy sites are having.

1.5 Parrot abundance and geophagy in southeastern Peru

Roughly twenty members of the parrot family inhabit the dense lowland tropical rainforest of southeastern Peru (Rainforest Expeditions 2001). These are (largest to smallest), blue and yellow macaw Ara ararauna, red and green macaw Ara chloroptera, scarlet macaw Ara macao, blue-headed macaw Ara couloni, red-bellied macaw Ara manilata, chestnut-fronted macaw Ara severa, mealy parrot Amazona farinosa, yellow-crowned parrot Amazona ochrocephala, blue-headed parrot Pionus menstruus, white-bellied parrot Pionites leucogaster, orange-cheeked parrot Pionopsitta barrabandi, white-eyed parakeet Aratinga leucophthalmus, dusky-headed parakeet Aratinga weddellii, black-headed parakeet Pyrrhura rupicola, painted parakeet Pyrrhura picta, cobalt-winged parakeet Brotogeris cyanoptera, scarlet- shoulded parrotlet Touit huetti, tui parakeet Brotogeris sanctithomae, Amazonian parrotlet Nannopsittaca dachilleae and dusky billed parrotlet Forpus sclateri (Rainforest Expeditions 2001). Only two species are on the IUCN Red List of globally threatened species, the blue-headed macaw Ara couloni (endangered) and Amazonian parrotlet Nannopsittaca dachilleae (near-threatened) (IUCN 2007). The reason for this diversity in parrot species is due to the varied habitats and food sources that are to be found in lowland tropical rainforests (Terborgh et al 1990). This allows for vast amounts of evolutionary diversity to occur over other habitats that have fewer and less varied food sources available.

As seen in afore mentioned literature on parrot geophagy, it is vital for some parrots to consume soil or clay as a regular part of their diet (Brightsmith et al 2004, Gilardi et al 1999). This is true for many species that inhabit southeastern Peru. As such there

14 are many macaw, parrot and parakeet clay-lick sites, locally called colpas (referred to as in remaining literature), to be found in the area. These are usually located on exposed sections of river bank kept free from vegetation by erosion from the river, but can also be found inland in some cases. Locally the colpas are used on a daily basis by feeding birds and this regularity has led to extensive research been undertaken at certain sites (Tambopata Research Centre, the largest macaw colpa in the world, studied for over 15 years). It has also led to the development of ecotourism in the area with many lodges been built to cater for tourists who want to observe rainforest flora and fauna. Excursions to observe the many species of parrot that utilize colpas in the region are an integral part of this. Due to these factors it is an ideal location to perform a study on the extent of human disturbances at a parrot geophagy site.

1.6 Ecotourism and parrots in Peru

Ecotourism is hard to define, but can losely be described as “nature-based tourism, which is protective of nature as well as enjoying it” (Valentine 1992). The use of the term “ecotourism” can only be traced back as far as the late 1980s as a reaction to the negative impacts of mass tourism to natural areas (Richardson 1993). An ecotourist should be seen to practise a non-comsumptive use of wildlife and natural resources, and contribute to the visited area through labour or financial means, aimed at directly benifiting the conservation of the site (Ziffer 1989).

Since the 1970s ecotourism has been expanding in Peru. The country has varying habitat types from high-altitude mountain ranges and altiplano, to dense, lowland tropical rainforest. This combined with a deep anthropological history ensures that Peru is a magnet for many travellers. Ecotourism in the Peruvian Amazon has been used as a way to enhance the value of intact wildlands, promote conservation and stabalise land- use patterns (Yu et al 1997). Many ecotourist lodges in the Peruvian Amazon rely on parrots and their associated geophagy behaviour as a selling point to visitors. This is due to the unique abundance and variety of parrot species that will reliably consume clay from known geophagy sites on a daily basis. As such many colpas in southeastern Peru will have associations with one or several lodges, who take tourists to observe parrots feeding. It is the disturbances caused to feeding birds during these visits that this study will be focusing on.

15 1.7 Effects of tourist visitation on parrot geophagy sites

There is very little known about the effects of tourist visitation on parrot colpa feeding behaviour. The quantity of clay and the time needed on geophagy sites for parrots to remain healthy is unknown. Due to this factor it is vital to try to minimise any disturbances that are attributed to tourist visitation. Studies on parrot geophagy sites have indicated that increased disturbances will result in a decrease in parrot abundance (Tatum-Hume et al 2004, Hammer 2002). It is not known how much this decrease affects parrot health, due to the possible effects of deficencies in clay usually sort from colpas. Different factors such as tourist arrival time and behaviour will all cause different levels of disturbance to any parrots present at the site. At this moment there are no studies quantifing tourist disturbances or highlighting the factors responsible for the most disturbance. Due to the importance of geophagy for many parrot species to survive and remain healthy, it is vital to understand any disturbances caused to them and try to reduce these factors to a minimum.

2.0 AIMS

The aim of this investigation is to evaluate tourism related disturbances on a parrot geophagy site in southeastern Peru. Boat, tourist and natural disturbances will all be analysed in order to identify the factors that attribute most disturbances to parrots on and around the colpa. The abundance and number of species will be recorded to assess which use the colpa and whether any are more susceptible to the certain disturbances. Management recommendations will then be made that will help to remove or at least reduce avoidable human disturbance factors. This will reduce the impacts that current visitation is having and benefit the whole parrot community that utilize the study site.

16 3.0 STUDY AREA

3.1 Peru

Peru, officially the Republic of Peru, is the world’s 20th largest country, with a landmass of 1,285,220 km2 (BBC 2007). It borders Ecuador and Columbia to the north, Brazil and Bolivia to the east and Chile to the south (Figure 1). To the west lies the Pacific Ocean. It has a population of over 28 million people (United Nations 2004), who speak Spanish, with others bilingual in Quechua, Aymara or other native languages. Eastern Peru consists mostly of the moist tropical rainforest of the Amazon Basin whilst western areas are dominated by the Andes mountain range and other high altitude habitats.

Figure 1: Map of Peru showing location of study site (BBC 2007).

3.2 Study site

The study was carried out at the La Torre colpa (S 12° 49’38, 09’, W 69° 17’23, 49’) on the river Tambopata, southeastern Peru (Figure 2). The site is roughly 2 hours by boat upstream of the town of Puerto Maldonado (Figure 1), which is located on the confluence of the Amazonian rivers of Madre de Dios and Tambopata (S 12° 36’12, 55’, W 69° 11’31, 79’). It is in the tropical zone 205 metres above sea level, in the Department of Madre de Dios, near to the borders of Brazil and Bolivia. The colpa is situated on the edge of the Tambopata-Candamo Reserve Zone (TCRZ) that originated in the 1970s. Initially it comprised about 5,000 hectares but this area was enlarged to 1.5 million hectares in 1990. The TCRZ is spread over two Departments, that of Madre de Dios (Province of Tambopata), and Puno (Provinces of Carabaya y Sandia), and covers approximately 1.5 million hectares. Habitats range from sub-tropical moist

17 forest, to cloud forest and tropical savannah (Hammer 2002). Rainfall averages 2,000 mm per year and humidity is roughly 75%.

Figure 2: Satellite image of the Tambopata , La Torre colpa, Inotawa Lodge and Posada Amazonas (GoogleEarth 2007).

3.3 The La Torre colpa

The La Torre colpa is a small, exposed clay cliff set back from the river Tambopata’s eastward bank by 20-25 metres (Figure 2). At this point the river is roughly 50 m wide. The cliff is approximately 5-8 m high and 15m wide (Figure 3). A broad sandy beach made up of fluvial deposits runs for a width of 6-10 m for approximately 30 m along the river’s edge. This is predominantly exposed but after heavy rainfall becomes flooded. The beach is backed by dense secondary rainforest consisting mainly of a variety of palms (Palmaceae), Cercropia and Balsa (Ochroma). The colpa is only visable from about 25 m on either side. However it is exposed and visable from the river and opposite dank due to a depression that is directly in front of the cliff face (approximatly 30 m2). This is mainly vegetated by understory species such as heliconia (Heliconiacae) and legume (Leguminosae). The colpa is used by two lodges in the area and as such two blinds have been constructed to allow for tourist visitation. These are situated 20 m to the left of the colpa, both having capacity for 8-12 people.

Figure 3: Veiw of the La Torre colpa from the Inotawa Blind (Authors photograph).

3.4 Tourist visitation

18 There are two lodges in the area that use the La Torre colpa. Inotawa Lodge is situated roughly 500 m downstream of the colpa (Figure 2), on the westward side of the river Tambopata (S 12° 48’36,87’, W 69° 18’11,32’). The lodge has capacity for 30 people and provides ecotourists with the opportunity to observe different varieties of rainforest flora and fauna. This includes guided walks through the forest, observing different forms of native cultervation, and visiting the colpa to watch macaws, parrots and parakeets. In peak tourist season the blind is used nearly everyday with variations in tourist numbers depending on group size. In the off season the blind is used approxinatly every 2-3 days depending on numbers of tourists staying at Inotawa.

Posada Amazonas (Figure 2), is much larger than Inotawa Lodge with 30 rooms and a capacity of 100 people (S 12° 48’08,22’, W 69° 17’59,37’). It is situated approximatly 20 minutes walk from the colpa on the eastward side of the river Tambopata. It Opened in 1998 and is run by Rainforest Expeditions (Est. 1989). It is part of a community partnership ecotourism project that is jointly owned by the local Ese-Eja community of Infierno, and is situated inside the communities private reserve on the eastward side of the river (Rainforest Expeditions 2006). It offers similar trips to Inotawa and also has a blind at the La Torre colpa. The Posada blind is situated next to the Inotawa’s 20 m left of the colpa. It is used most days during the peak season, with visitation numbers to the colpa varying according to how many people are staying at the lodge.

4.0 METHODOLOGY

4.1 Parrot observations

The study was conducted in early July 2006 over a 28-day period, with a total of 24 observation days. Recordings of parrot species and abundance were made from the Inotawa blind using a data sheet designed for the Tambopata Research Project (Appendix 1). The species and number of birds feeding were recorded using five- minute counts (Brightsmith 2004). The moment the first bird of the day landed on the colpa a one-minute count of the species feeding and number of individuals involved

19 was started. A gap of 4 minutes was then left until another one-minute count was started. This was repeated until all birds had left the colpa and surrounding trees. This method allowed for identification of variation in abundance between days of high and low disturbance. Observations were made using binoculars and Tambopata area parrot field guide to ensure accurate species and number recognition (Rainforest Expeditions). Arrival at the study site was by canoe, approximately 6 AM (EST) just before sunrise. This was to ensure arrival before any tourists and to cause as little disturbance to any birds that may have already been present. Departure time from the site was roughly 9-10 AM (EST), half an hour after the last bird to leave the study area. This was to ensure that feeding activities at the colpa had totally finished.

4.2 General disturbances

Disturbances to parrots were divided into four broad categories: tourist disturbances, boat disturbances, animal disturbances and unknown disturbances. Parrot flushes were used as an indicator of disturbance. A flush is when a congregation of birds suddenly takes flight from a settled position (Bessinger & Casagrande 1997), in this case on the colpa or surrounding trees. These were recorded in order to assess the effects of disturbances on feeding and non-feeding birds.

4.3 Tourist disturbances

Tourist disturbances were divided into arrival/departure, quiet talking, loud talking, dropped object and cough/sneeze. Every time one of these factors occurred any associated flushes from the colpa or surrounding trees were recorded. Any species and the number of individuals involved in the flush were also recorded. This was to ensure accurate identification of the tourist factor that caused the most disturbances, and whether any species is affected more than another.

4.4 Boat disturbances

20 Boat disturbance was divided into three different factors; loud boat not stopping, quiet boat not stopping and tourist boat stopping. Loud boats were classed as those that used traditional peke-peke motors (8-16 BHP), quiet boats were ones that used more modern outboard motors, and tourist boats were recorded as any boat that was used at the pick-up point on the beach, for tourist arrival and departure. Any boat disturbance factor that caused a flush to birds on the colpa or in the surrounding trees was recorded. The species and number of individuals involved were also recorded. This was used when establishing whether one boat disturbance factor was affecting the birds more than another, and whether any species were particularly affected.

4.5 Animal disturbances

Animal disturbance was recorded as any flushes caused to birds on the colpa or in the surrounding trees by wildlife that occurs naturally in the surrounding area, such as monkeys, birds of prey and snakes. When a flush was caused in this way any species and the numbers of individuals involved were recorded. This was used to establish the extent of natural animal disturbance caused to the parrots that use this site.

4.6 Unknown disturbances

Unknown disturbances were classed as flushes by birds on the colpa or in the surrounding trees without any obvious association with any of the disturbance factors already listed in this study. When this was observed, any species involved and the numbers of individuals were recorded to establish the amount of apparently unknown disturbances.

4.7 Statistical analysis

4.7a. Associations

Associations of species and species associations with disturbances were calculated using Spearman’s rank correlation coefficient (Wheater & Cook 2000). This is a non- parametric correlation analysis for examining relationships between two variables. Each variable is ranked separately and comparison then takes place (Wheater et al

21 2000). A P value of less than 0.01 shows a highly significant difference between variables, less than 0.05 is a significant difference and a P value greater than 0.05 shows no significant difference between variables.

4.7b. Variances between disturbance factors

Variances between the different disturbance factors and amount of disturbance caused to birds on the colpa and surrounding trees was calculated using Kruskal-Wallis one- way ANOVA analysis. This is a non-parametric statistical test to examine differences between more than two samples comprising unmatched, independent data (Wheater et al 2000). Any significant or non-significant differences between data sets will be highlighted using P value results.

5.0 RESULTS

5.1 Numbers recorded

Parrot numbers feeding on the colpa were recorded over a 28-day period with a total of 24 observation days. Overall 8 species of parrot were recorded feeding on the colpa, these were red and green macaw Ara chloroptera, chestnut-fronted macaw Ara severa, mealy parrot Amazona farinosa, yellow-crowned parrot Amazona ochrocephala, blue- headed parrot Pionus menstruus, orange-cheeked parrot Pionopsitta barrabandi, dusky- headed parakeet Aratinga weddellii and white-eyed Parakeet Aratinga leucophthalmus (for general information see Appendix 2). In total, 775 individuals were recorded feeding on the colpa (Table 1). Dusky-headed parakeet Aratinga weddellii were the most commonly observed with 337 individuals recorded over the study period. Combined with 209 blue-headed parrot Pionus menstruus individuals they make up over 50% of total parrots recorded feeding. Red and green macaw was the least common with only 2 individuals being observed on day 27 (Table 1). Dusky-headed parakeets Aratinga weddellii had a mean value of 1.48 individuals recorded feeding per day (Table 2). This makes them the most commonly observed species feeding on the colpa. However, they show a high standard deviation of 1.33

22 suggesting high variability between visitation numbers per day. Blue-headed parrots Pionus menstruus record the second highest value with a mean of 0.74 (Table 2). Red and green macaw Ara chloroptera was the species with the lowest mean value recorded of 0.004 individuals per day, making it the least abundant species (Table 2). A standard deviation of 0.18 shows little variance in number of individuals observed between days.

Table 1: Total number of individual birds observed feeding by species/day.

Red and Chestnut Yellow Blue Orange Dusky White Mealy Day Green Fronted Crowned Headed Cheeked Headed Eyed Total: Parrot No. Macaw Macaw Parrot Parrot Parrot Parakeet Parakeet 1 0 0 0 0 0 0 0 0 0 2 0 0 0 0 7 0 21 0 28 3 0 0 4 2 13 0 14 5 38 4 0 2 1 2 2 0 0 0 7 5 0 2 6 1 13 3 19 7 51 6 0 3 3 3 21 2 23 3 58 7 0 0 0 0 2 0 14 0 16 8 0 0 0 0 7 0 16 0 23 9 0 0 0 1 4 0 6 0 11 10 0 0 0 0 12 0 4 16 32 11 0 0 0 0 2 0 11 0 13 12 0 0 1 2 9 0 7 0 19 13 0 2 0 1 10 0 5 2 20 14 0 0 13 6 10 0 27 6 62 15 0 18 5 0 17 2 32 0 74 16 0 0 0 0 0 0 2 0 2 17 0 1 0 0 0 0 0 0 1 18 0 4 5 7 12 0 14 0 42 23 0 25 0 2 22 0 0 0 49 24 0 13 2 7 8 0 29 0 59 25 0 11 2 3 21 0 13 1 51 26 0 0 0 2 0 0 11 0 13 27 2 8 1 5 8 1 35 0 60 28 0 1 0 2 9 0 34 0 46 Total: 2 90 43 46 209 8 337 40 775

Table 2: Mean number of individual birds observed feeding per day (± Standard Deviation).

23 Red and Chestnut Yellow Blue Orange Dusky White Mealy Species: Green Fronted Crowned Headed Cheeked Headed Eyed Parrot Macaw Macaw Parrot Parrot Parrot Parakeet Parakeet

0.0038 0.3730 0.1447 0.1441 0.7374 0.0345 1.4799 0.025 Mean: ± 0.18 ± 0.68 ± 0.26 ± 0.19 ± 0.74 ± 0.08 ± 1.33 ± 0.17

5.2 Species associations

Species associations were calculated using Spearman’s rank correlation analysis. Mealy parrot Amazona farinosa were the species most associated with other species feeding on the colpa (Table 3). They showed a correlation at 0.01 levels with dusky- headed parakeet Aratinga weddellii, blue-headed parrot Pionus menstruus and yellow- crowned parrot Amazona ochrocephala. At the 0.05 level correlations were seen with chestnut-fronted macaws Ara severa, orange-cheeked parrot Pionopsitta barrabandi and white-eyed parakeet Aratinga leucophthalmus (Table 3). Chestnut-fronted macaws were also strongly associated with other species being present. Associations were seen with blue-headed parrots Pionus menstruus and yellow-crowned parrots Amazona ochrocephala at the 0.01 level and at the 0.05 level correlations were seen with mealy-parrots Amazona farinosa and orange-cheeked parrots Pionopsitta barrabandi. White-eyed parakeets Aratinga leucophthalmus showed little species associations; only at 0.01 levels with mealy parrot Amazona farinosa and blue-headed parrot Pionus menstruus. Red and green macaw Ara chloroptera was the only species to have no associations (Table 3).

24 Table 3: Species associations using Spearman’s rank correlation (** = strongly associated * = associated).

Red and Chestnut Mealy Yellow Blue Orange Dusky Green Fronted Parrot Crowned Headed Cheeked Headed Macaw Macaw Parrot Parrot Parrot Parakeet White Eyed -0.13 -0.01 0.41* 0.11 0.51* 0.22 0.20 Parakeet p = 0.54 p = 0.99 p = 0.04 p = 0.63 p = 0.01 p = 0.30 p = 0.35 Dusky Headed 0.35 0.36 0.59** 0.46* 0.51* 0.51* Parakeet p = 0.10 p = 0.08 p = 0.01 p = 0.02 p = 0.01 p = 0.01 Orange Cheeked 0.39 0.49* 0.50* 0.10 0.42* Parrot p = 0.60 p = 0.02 p = 0.02 p = 0.64 p = 0.04 Blue Headed 0.20 0.67** 0.61** 0.51* Parrot p = 0.36 p = 0.00 p = 0.01 p = 0.01 Yellow Crowned 0.33 0.52** 0.53** Parrot p = 0.12 p = 0.01 p = 0.01

Mealy 0.05 0.44* Parrot p = 0.82 p = 0.03 Chestnut Fronted 0.24 Macaw p = 0.26

5.3 Parrot abundances and days of disturbance

Day 5 had the highest mean total parrot numbers with a value of 6.8 (Figure 4). On the same day an extremely low disturbance value of 0.2 was recorded. Day 1 and 17 have

25 the lowest mean value for total parrots, however recorded large disturbance figures of 0.8 and 1.0 respectively (Figure 4). These results seem to show links between low disturbance levels and high parrot visitation numbers. However the results are extremely varied over the whole study period. Day 27 recorded the second highest mean total parrot value of 6.2 but it also recorded the highest disturbance levels over the whole observation time with a figure of 1.5 (Figure 4).

Figure 4: Mean disturbance levels compared to mean parrot visitation numbers per day.

Mean Total Parrots Mean Disturbance

s 6.00 t o r r a P

o 5.00 T

n a e M / s

l 4.00 e v e L

a 3.00 b r u t s i D

a 2.00 e M

0.00 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 23 24 25 26 27 28 Day Number

5.4 Species associations with different disturbance factors

26 Species associations with disturbances were calculated using Spearman’s rank correlation analysis. Yellow-crowned parrot Amazona ochrocephala and white-eyed parakeet Aratinga leucophthalmus were the only species to show any correlation with any disturbance factors (Table 4). Amazona ochrocephala were correlated at the 0.05 level with boat disturbances and at the 0.01 level with tourist disturbances. Aratinga leucophthalmus were also correlated with tourist and boat disturbance but only at 0.01 levels (Table 4). No species showed any association with animal disturbances. The results of unknown disturbances were minimal and no data analysis has taken place.

Table 4: Species/disturbance associations calculated using the Spearman’s rank correlation (** = strongly associated * = associated). Red and Chestnut Mealy Yellow Blue Orange Dusky White All Green Fronted Parrot Crowned Headed Cheeked Headed Eyed Parrots Macaw Macaw Parrot Parrot Parrot Parakeet Parakeet

Boat +0.26 +0.24 -0.12 +0.52** -0.06 -0.30 +0.20 -0.45* +0.15 Disturbance p = 0.23 p = 0.26 p = 0.57 p = 0.01 p = 0.79 p = 0.15 p = 0.35 p = 0.03 p = 0.47

People +0.35 +0.21 -0.17 +0.44* -0.15 -0.30 -0.07 -0.48* -0.78 Disturbance p = 0.10 p = 0.33 p = 0.43 p = 0.03 p = 0.48 p = 0.16 p = 0.73 p = 0.02 p = 0.71

Animal -0.16 +0.11 +0.01 -0.07 +0.02 +0.11 -0.01 -0.17 +0.03 Disturbance p = 0.47 p = 0.60 p = 0.10 p = 0.76 p = 0.94 p = 0.63 p = 0.97 p = 0.44 p = 0.90

5.5 General disturbance factors

Non-parametric tests using Kruskal-Wallis analysis shows a significant difference between the general disturbance types and bird disturbance (flushes from trees X2 = 52.9 df = 3 P = <0.001, flushes from colpa X2 = 63.3 df = 3 P = <0.001). Boats attributed the

27 least disturbances to both birds in trees and on the colpa, with low means of 1.25 and 0.18 respectively (Table 5). Tourist disturbances were responsible for the greatest amount of overall bird disturbance, with large mean values of 3.04 flushes from trees and 2.85 flushes from the colpa (Table 5). Animal disturbances had a high mean value of 3.33 flushes from trees, but a low value of 1.67 from the colpa. Both means for animal disturbance have high standard deviations indicating that animal disturbances resulted in variation between flushes in the trees and colpa (Table 5).

Table 5: Mean and standard deviation values comparing general disturbance factors with tree and colpa flushes.

Flush From Flush From Trees Colpa Boats Mean 1.25 0.18 (N = 103) Std. Dev 1.22 0.76 Tourist Mean 3.04 2.85 (N = 46) Std. Dev 1.56 2.27 Animal Mean 3.33 1.67 (N = 3) Std. Dev 2.08 2.90 Unknown Mean 3.40 2.60 (N = 15) Std. Dev 1.30 2.29

5.6 Tourist disturbance factors

Results of the tourist disturbance factors examined in this study, using Kruskal-Wallis non-parametric analysis, shows there is no significant difference between different tourist disturbance types and flushes from trees or the colpa (flushes from trees X2 = 0.486 df = 4 P = 0.975, flushes from colpa X2 = 9.908 df = 4 P = 0.042). Mean analysis of tourist attributed flushes show varied disturbance types affect birds in the trees and on the colpa differently. Quiet talking had a mean value of 3 flushes from the trees compared to a 0 value of flushes from the colpa (Table 6). Coughing and sneezing were the largest disturbance factor overall with mean figures of 3.75 from the colpa and 3.5 from the surrounding trees (Table 6). Loud talking affected birds on the colpa the most recording a mean of 3.95. The least disturbance caused was by the arrival and departure of tourists, however a high standard deviation of 2.52 for colpa flushes shows variances in disturbance between days.

28 Table 6: Mean and standard deviation values comparing tourist disturbance factors with tree and colpa flushes. Human disturbance factor: Flush from trees Flush from colpa Mean 3.00 0.00 Quiet talking (N = 3) Std. Dev 2 0 Mean 3.06 3.95 Loud talking (N = 18) Std. Dev 1.35 1.59 Mean 3.5 3.75 Cough/sneeze (N = 4) Std. Dev 1.74 2.5 Mean 3.00 2.33 Dropped object (N = 9) Std. Dev 1.21 2.30 Mean 2.82 1.82 Arrival/departure (N = 11) Std. Dev 1.10 2.52

5.7 Boat disturbance factors

Kruskal-Wallace non-parametric analysis shows there is no significant difference between boat disturbances and flushes from trees or the colpa (flushes from trees X2 = 2.391 df = 2 P = 0.302, flushes from colpa X2 = 5.487 df = 2 P = 0.064). Mean analysis shows that loud boats not stopping was the boat disturbance factor that affected birds on the colpa and surrounding trees the most (Table 7). Tourist boats not stopping and quiet boats stopping both have low mean disturbance values for colpa flushes. Quiet boats not stopping caused the least disturbance to birds in the trees (Table 7). Tourist boats stopping have a higher mean disturbance value for tree flushes but a lower standard deviation, indicating variability in bird reactions to different boat disturbance.

29 Table 7: Mean and standard deviation values comparing boat disturbance with tree and colpa flushes. Human disturbance Type: Flush from trees Flush from colpa Quiet boat not Mean 1.11 0.18 stopping (N = 56) Std. Dev 1.22 0.72 Loud boat not Mean 1.63 0.88 stopping (N = 8) Std. Dev 1.77 1.81 Tourist boat stopping Mean 1.38 0.06 (N = 103) Std. Dev 1.10 0.32

6.0 DISCUSSION

6.1 Abundance

6.1a. Most abundant species

In total eight parrot species were recorded consuming clay from the La Torre colpa. Dusky-headed parakeet Aratinga weddellii and blue-headed parrot Pionus menstruus were the two most abundant species to use the study site, with 337 and 209 individuals respectively recorded over the study period. Numbers feeding per day varied from 0- 34 Aratinga weddellii and 0-22 Pionus menstruus. This is similar to group sizes recorded from other similar sites in the area (Hammer 2002, Brightsmith 2004). On days when both species were absent from the colpa very low numbers of other species were recorded. This is because larger species rely on Aratinga weddellii and Pionus menstruus as an indicator of danger on or around the colpa, due to their relatively smaller size and therefore increased risk of predation (Burger et al 2003, Blumstein et al 2005). Hammer (2000) also recorded this use of “lead” species when studying a similar colpa in the El Gato region of the TCRZ.

6.1b. Least abundant species

Red and green macaw Ara chloroptera was the least abundant species observed using the colpa, with only 2 individuals being recorded on one day. This is due to its large

30 size and the relatively small size of the colpa. Larger colpas in the area attract vast gatherings of Ara chloroptera, and other large macaw species (Brightsmith et al 2004, Tatum-Hume et al 2003). Larger macaw species have slower reaction times than the smaller parrots and parakeets, so favour colpas with a large surface area, allowing for easier predator vigilance and escape (Renton 2002).

6.1c. General abundance of species

Mealy parrot Amazona farinosa, yellow-crowned parrot Amazona ochrocephala, orange-cheeked parrot Pionopsitta barrabandi and white-eyed parakeet Aratinga leucophthalmus all were similar in abundance to each other. Each species had some days when no individuals were present and other days when 5-20 individuals would use the colpa. This may be due to the fact that there are several colpas in the immediate area that the birds can visit with no preference over which one (Duffie 2003, Brightsmith et al 2004). All these species are similar in body size (Appendix 2), and are smaller than the least abundant species Ara chloroptera, and larger than the smallest and most abundant species of Aratinga weddellii. This shows how this small colpa is dominated by parrot and parakeet species over larger macaws. As said in the above literature large macaws do not use this colpa due to fear of predation (Renton 2002). Studies into avian behaviour at limited resources show that larger macaw and parrot species may act aggressively towards other smaller, less dominate species (Burger et al 2003, Mac Nally et al 2005). The lack of these larger species and associated aggression can explain the large abundance of smaller species using this colpa (Burger et al 2003). This is similar to other studies, where sites with a smaller surface area are dominated by smaller species, whilst others with a larger and more exposed area have the most abundance occurring in larger species (Tatum-Hume et al 2003, Duffie 2003, Gilardi et al 1998). 6.2 Species associations

Species association was calculated using Spearman’s rank correlation analysis. All species recorded apart from red and green macaw Ara chloroptera showed association with blue-headed parrot Pionus menstruus and dusky-headed parakeet Aratinga weddellii. These were present most observation days and were usually one of the first and most confident species to land on the colpa (pers. obs), as is the same from studies

31 into similar sites (Duffie 2003, Hammer 2002, Brightsmith 2004). This links with the abundance data, as when these species were absent from the colpa, very low abundances were recorded for the other species. This seems to prove that the larger species are relying on these smaller, more predatory at risk species as indicators of safety (Lima et al 1999, Karubian et al 2005). This has also been recorded in research into other avian species feeding behaviour (Morse 1977, Brown 1969). With relevance to this study it is obviously vital that disturbances cannot reach the level where they completely deter Pionus menstruus and Aratinga weddellii from feeding. If this happens the other species that use this colpa will not feed.

6.3 Species interdependence

In general associations were seen amongst all species, except for red and green macaw Ara chloroptera, owing to it only being observed on one day. The associations shown between the other species in this study illustrates how interdependent on one another they are as indicators of safety (Lima et al 1999, Hilton et al 1999). This is explained by the decreased risk of predation when flocking behaviour is adopted, due to collective vigilance, dilution of risk and predator confusion (Hilton et al 1999, Barbosa 1997, Szekely et al 1989). This is important when considering disturbance factors at this site, as a disturbance that deters one species, will consequently help to deter another through its lack of presence.

6.4 General disturbance and parrot abundance

Mean disturbance levels show very little correlation with parrot abundance. Some days with high mean disturbance levels still recorded high parrot visitation numbers. This indicates that it is not the general level of disturbance but certain disturbance factors that influence parrot abundance on the colpa. Previous studies on the effects of human disturbance on avian behaviour have highlighted this (Webb et al 2005, Lafferty 2004), as well as the need to identify the key factors that cause the most disturbances (Guillemain et al 2007, Heil et al 2006, Stillman et al 2007).

6.4a. Associations with general disturbance factors

32 Only two out of the eight parrot species in this study showed any associations with the three main disturbance factors tested (boat, tourist or animal). Flushes by yellow- crowned parrot Amazona ochrocephala and white-eyed parakeet Aratinga leucophthalmus were correlated with boat traffic and tourists. It has been well documented that boat traffic and human presence do negativly affect bird abundance and behaviour (Stalmaster et al 1997, Bratton 1990). However, it has also been shown that there is variation in response to disturbance between different species (Gill et al 1999). This depends on their natural reaction to predation and species life history in the area (Hansen et al 1992). In this case Amazona ochrocephala and Aratinga leucophthalmus species may associate boats and people with increased danger due to previous exploitation by humans (Burger et al 2003). This may explain their more extreme reactions to tourist and boat disturbance over the other parrot species studied.

6.4b. Differences observed between general disturbance factors

A significant difference was found between disturbance type (boat, tourist, animal) and overall bird disturbance. Boats caused the least disturbance whilst tourists caused the most. This stretch of the River Tambopata is used regularly by boat traffic with an average of about 8 boats going past the colpa during each day of observation (pers. obs). The lack of overall reaction suggests that some habituation to boat disturbance has taken place in the species recorded at this site (Carney et al 1999). This has been illustrated in other studies of repeated boat disturbance on avian species (Burger et al 2003, Guillemain et al 2007). Animal disturbance only recorded three incidences over the study period, accounting for a very small percentage of overall disturbances. This makes this irrelevant to this study, as they are not a major disturbance issue at this site. When considering management implications for this site this needs to be taken into account, as tourists are disturbing birds the most.

6.5 Tourist disturbance factors

6.5a. Cough/sneeze and dropped objects

Tourist disturbance factors were split into five categories; Arrival/departure, quiet talking, loud talking, cough/sneeze and dropped object. Overall coughing and sneezing

33 were the factors that caused the most disturbances to birds on or around the colpa. These types of disturbances can be classified as “impulse” noises, due being non- continuous and originating suddenly (Larkin 1996). Extensive research undertaken on the subject has been focused mainly on the effects of military impulse noises such as artillery and gunfire (Tazik et al 1992, Schomer 1994). These have shown that impulse noises cause greater disturbance to wildlife than continuous levels of sound (Tazik et al 1992, Schomer 1994, Pater et al 1999, Larkin 1996). Dropped objects can also be classed as impulse noises, and in this study resulted in relatively large amounts of disturbance to birds on the colpa and in the trees. This highlights the need for the reduction in impulse noises when observing parrots at the colpa to minimise disturbance.

6.5b. Loud talking

Loud talking was the most commonly recorded tourist factor, and disturbed birds on the colpa and surrounding trees to similar levels. Loud talking can be described as a continuous noise but also has impulse noise properties due to its often-sudden onset (Surman 2006). Flushes were caused at the start of loud conversations, and commonly resettlement into at least the surrounding trees took place whilst the talking continued (pers. obs.). Other studies into noise disturbance on birds have found similar behaviour to occur in the European starling Sturnus vulgaris (Rich et al 2005) and marbled murrelet Brachyramphus marmoratus (Singer et al 1995). This indicates that some habituation to the levels of noise has taken place but the natural response to the sudden onset of loud talking is still present. This needs to be considered in this study as loud talking forced birds of the colpa and therefore reduced their feeding time.

6.5c. Quiet talking

Quiet talking was the least disturbing of the tourist factors analysed in this study. Birds feeding on the colpa saw no reaction, and only minor reactions were seen to birds in the surrounding trees. This can be attributed to parrot habituation to tourist visitation at this site (Yorio et al 2001). This has been well documented in other avian species where blinds are used for tourist observation (Walker et al 2006, Bouton et al 2005,

34 Hidinger 1996). Quiet talking can be described as a continuous noise factor with no defining start and finish (Larkin 1996). As seen in the above literature continuous noise factors cause fewer disturbances to birds than sudden impulse noises (Tazik et al 1992, Schomer 1994, Pater et al 1999). This has been illustrated in this study when comparing parrot reactions to coughing and sneezing with reactions to quiet talking.

6.5d. Arrival/Departure

Tourist arrival and departure resulted in minimal disturbances to the various species studied at this site. Disturbance was minimised to feeding birds by tourist arrival usually being before feeding had started and departure once feeding had finished (pers. obs). This meant that there were few, if any birds in the area when these activities were taking place. It also meant that most birds arrived after tourist settlement into the blinds had occurred. This has been found to significantly reduce the impact of humans at other wildlife study sites (Tershey et al 2002, Wasser et al 1997). Birds in the trees showed some responses but reactions were not as strong as with the other disturbance factors of loud talking, dropped object or coughing/sneezing. These responses (or lack of) can be attributed to the habituation of human activity at the landing site on the beach (Pfeiffer 2004). Reduced reactions to disturbances caused by the arrival and departure of tourists from the same frequently used point have been recorded from similar studies into the effects of human disturbance (Yosef 2000, Pitts 2001, Grossberg et al 2003). Intolerance of tourists has been observed from other wildlife studies and is usually marked with a decline in abundance of the species concerned (Enzenbacher 1994, Tershy et al 1997). However the continuous use of this colpa by various parrot species indicates that the disturbances attributed to tourist arrival and departure does not unduly deter birds from feeding.

6.6 Boat disturbance

6.6a. Loud boats not stopping

Disturbances by boats were assessed by noise, and whether or not they stopped at the beach in front of the colpa. Quiet boats were classed as ones that used outboard motors and loud boats were ones that used more traditional peke-peke motors. Loud boats

35 going past the colpa resulted in the most flushes to feeding birds as well those perched waiting to feed. This was the least common form of boat disturbance and may account for increased bird reactions due to habituation to the other forms (Belanger et al 1989).

Peke-peke motors are significantly louder and deeper in pitch than outboard motors (pers. obs). Research shows that it is a combination of both the sound and sight of boats that causes disturbance, with increased reactions to fast moving power boats over quieter, slower moving vessels, such as sail boats or canoes (Rogers et al 2002, Mosisch et al 1998). The length of disturbance time is increased with peke-peke motors as they are slower and take longer to pass the colpa (pers. obs). This increases exposure time to human sight and sound disturbance and therefore gives more time for a flush reaction to take place (Draulans et al 1985, Gill et al 1999). Species life history may also be taken into account when considering boat disturbance. The species in this study may associate the traditionally used peke-peke motor with previous hunting and exploitation (Martin 1995, Hansen et al 1992). Increased reactions to this type of disturbance may have been passed from generation to generation contributing to the lesser reaction to newer outboard motors over traditional peke-peke (Dobson 1989).

6.6b. Quiet boats not stopping

This factor resulted in the least disturbance to birds in the trees, and birds on the colpa showed only minor reactions. Disturbance levels varied in scale with some days having only a few boats going past whilst others recorded more than ten incidences. The high level of use of the river for transport and tourist lodges can account for this (pers. obs.), with decreased bird reactions been attributed to the habituation of outboard powered boats (Bright et al 2003). Literature about boat disturbance on parrots is limited, but habituation of this type has been recorded amongst many other aviforme species (Vos et al 1985, Watson et al 1999, Newbrey et al 2005, Peters et al 2007). As written above, the decreased volume of outboard motors compared to peke- peke’s will also have affected parrot behaviour, due to increased flush reactions caused by louder, longer lasting peke-peke disturbance events (Draulans et al 1985, Gill et al 1999).

6.6c. Tourist boats stopping

36 This factor caused the least disturbance to birds on the colpa and resulted in minimal disturbance to birds in the surrounding trees. As seen when considering tourist disturbances in the above sections, the lack of reaction by birds on the colpa was due to the times of tourist arrival and departure (Tershey et al 2002, Wasser et al 1997). Arrival would usually be before any birds had started feeding and departure would usually be after all the birds had stopped feeding (pers. obs.). This resulted in the minimum of disturbance to feeding birds. Disturbance to birds in the surrounding trees was greater than that of quiet boats not stopping but less than that of loud boats not stopping. The close proximity (within 30 m of the colpa) of the landing site and clear view of tourist activities by perched birds would have attributed to this (Fernadez- Juricic et al 2001, Hill et al 1997). However, the lack of overall negative reactions to tourist boats landing indicates tolerance and habituation to these activities (Burger et al 2003). This behaviour has been found to occur commonly in many bird species exposed to high rates of tourist visitation (Carney et al 1999, Bright et al 2003, Watson et al 1999)

6.7 Limitations of the study

This study was relatively successful in establishing the main effects that tourist visitation is having on at this site, however there are improvements that could be made in future research. More analysis of tourist disturbances should take place, such as amount of activity in the blind and colour of clothing worn. These factors may influence parrot behaviour due to their being some outside visibility into the blind. If a future study was to take place more information on boat disturbances should be gathered. This should include clear identification of who is responsible for the boat, whether it be tourist lodges or locals. This can then be used to clearly establish the effects of the many tour-operated boats that rely on the river to transport guests. Identification is needed on the actual quantity of clay certain parrot species need to consume to remain healthy. This is currently unknown and it is therefore hard to assess whether parrots are actually consuming enough clay. A better understanding of this would greatly improve the current knowledge of the effects of tourism on parrot behaviour at geophagy sites.

37 6.8 Management implications

6.8a. Abundance of species

Research into geophagy in parrot species has illustrated the importance and necessity of this activity in order to survive and remain healthy (Brightsmith et al 2004, Gilardi et al 1999). If disturbances were too great birds would be driven away to other quieter colpas in the area, or at worst possibly not feed at all. In this study, general boat and tourist disturbances didn’t seem to be deterring feeding parrots at this site. The study illustrates that on days with high disturbances recorded, high parrot visitation and feeding numbers could also be observed. The species that utilize this site are fairly common and none are threatened in the near future (IUCN 2007). Key species such as Aratinga weddelli and Pionus menstuus need to have their presence maintained at this site in order to attract other species. This site can continue to be used for tourist visitation, as disturbances caused are not unduly deterring the various parrot species from feeding.

6.8b. Tourist disturbances

There are few papers available on the impacts of tourist visitation to parrot geophagy sites (Tatum-Hume et al 2004, Duffie 2003, Hammer 2002). The results of this study have highlighted factors that cause the most disturbances to feeding and perched birds at the La Torre colpa. Impulse noises such as coughing/sneezing, dropping objects and the onset of loud talking are all clearly identified as major sources of tourist disturbance. Although little can be done about coughing/sneezing simple measures could be taken to reduce the impact of other tourist created impulse noises. A tougher policy and enforcement of talking volumes when observing parrots from the blinds should be employed. During this study, some tour guides from the lodges were good at controlling sound levels coming from the blind, but others were not. This study has demonstrated that quiet talking does not cause significant amounts of disturbance. Therefore tighter control of noise volume at a quiet level would significantly reduce the disturbance that tourist visitation is currently having. Inotawa Lodge and Posada Amazonas could easily do this, by informing tourist guides of appropriate talking

38 levels and making sure they enforce them. As well as loud talking, dropped objects also represented a significant proportion of tourist created disturbance. There is little that can be done about this, as it usually resulted from clumsiness and accidents. However, padding of some sort could be used as a floor cover in the blind, on top of the wooden planks that are currently in place. This would provide some insulation from dropped objects and hopefully reduce the impact that this type of disturbance is having.

6.8c. Boat disturbances

There has been much research undertaken on the impacts of boat disturbance on avian species such as waterfowl and shorebirds (Belanger & Bedard 1989, Lafferty 2004, Stillman et la 2007). However there have been few studies on the impacts of boat disturbance to feeding parrots at geophagy sites (Tatum-Hume et al 2004). In terms of the management implications of this study there is little that can be done about boat disturbance. Arrival and departure of tourists was usually before and after any birds had started feeding, so the impacts of this activity had already been reduced as much as possible. Boats that used quiet, outboard motors (usually operated by a tourist lodge) caused very little disturbance to feeding birds. Studies have however shown that increases in boat traffic in the future could be enough to deter birds from feeding permanently (Tatum-Hume et al 2003). Monitoring the levels of boat traffic on the river should be undertaken to ensure it remains under control. Boats using peke-peke motors caused the most disruption to parrots at this site. As these are mostly used by locals there are limited options when considering management implications for this factor. Local people in the area cannot afford newer outboard motors, so there is no option for the discontinuation of peke-peke use. Education and information about this site and other sites in the area could be provided to locals with recommendations for speed limits and passing distances (Fernadez-Juricic 2001). This has been shown to work in other situations where boat disturbance is affecting wildlife (Bratton 1990). Inotawa and Posada, as a way of helping to insure that parrots are not driven away from the colpa, could provide this.

39 7.0 CONCLUSION

This study has highlighted the clear necessity of geophagy in the parrot species that use the La Torre colpa. It has also identified the tourism related factors that are responsible for the most disturbances to birds using the site. Analysis of these has shown that management strategies can be put into place to reduce the amount of disturbances that are currently occurring. Simple guidelines on sound levels when observing the colpa and floor padding to reduce the impact of dropped objects, would dramatically reduce the amount of disturbance that tourist visitation is contributing. Boat disturbance affected birds to a lesser degree than tourist visitation. Habituation to quiet boats and the times of tourist arrival and departure meant that few disturbances could be associated with these factors. Locally run boats with peke-peke motors were the boat factor most associated with disturbance. It is not economically viable to discontinue the use of these so information needs to be provided about the importance and location of colpa sites, appropriate speed limits and passing distances. This should jointly be undertaken by the lodges along the river that rely on the tourism provided by the many parrot geophagy sites in the area. Future research into other tourist disturbance factors and tourism related boat traffic should be undertaken to help further the current knowledge on tourism disturbances at geophagy sites. This should be accompanied by studies into the quantity of clay and the time needed to consume enough to maintain parrot health. If these suggested management strategies are implicated disturbances to the many parrot species that consume clay on the La Torre colpa can be better understood. This will help to reduce the effects that tourism at this site and others like it is having.

8.0 Acknowledgments

Thanks to my project supervisor, Dr. Stuart Marsden, for all the expert help and advice kindly given to me throughout this project, even at times when he didn’t have to. Alan Lee for putting up with me trying to learn parrot calls and identification in the field, as well as providing an excellent data sheet to use during my study. Lastly I would like

40 thank Rolando, Maria and Frieda, the family I stayed with when conducting my field research, they made me very welcome.

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10.0 Appendices

Appendix 1: Example of data sheet used to record parrot abundances and flushes (provided by Alan Lee)

51 Appendix 2: General information about the parrot species recorded at the La Torre colpa