**5. Environmental impacts and conservation threats**

#### **5.1 Habitat loss, degradation and fragmentation**

Birds are closely associated with forests, and approximately 30% of the world's species of birds are highly restricted to tropical forests used as either winter grounds or year-round habitats (Myers 1992). In Ecuador, Western and Tumbesian forests of Ecuador are being cleared by farming and ranching and are highly threatened by browsing and trampling of domestic livestock, with about 4% of the original forest coverage remaining by 1998 (Dodson & Gentry, 1991; Best & Kessler, 1995). For instance, uncontrolled cattle grazing of the native vegetation, deforestation, and agricultural sprawl (rice crops and farms) have negatively impacted the El Canclon Lagoon at the MCER, jeopardizing its conservation and affecting the local population of the Horned Screamer (*A. cornuta*) and several other waterbirds depending on this wetland (Alava et al., 2007; Alava et al., 2009). Likewise, it is estimated that about 55,400 hectares (27% of the original total area: 203,625 hectares) of mangrove forests has been lost in coastal Ecuador from 1969 to 2006 due to uncontrolled clear-cutting of mangroves (Fig. 4), not only for construction of illegal shrimp farms (aquaculture), but for agriculture, illegal extraction of timber and urban sprawl (CLIRSEN, 2007; Carvajal & Alava, 2007). The decrease of slat flat areas is also of concern with a reduction of 93% since 1969 (Fig. 4). Extensive banana plantations are found in southwest Ecuador, and are primarily located in coastal provinces such as Los Rios, El Guayas and the El Oro (INEC 2007). A total area averaging 232,235 ha is dedicated to the production of bananas at the national level. About 79% of this total are located on the coastal zone, mainly in the El Guayas and the El Oro provinces (an average of 51,183 and 44,607 ha, respectively), which are relatively close to mangrove areas. Presence of solid wastes (i.e., plastic bags and bottles) and illegal camp fires are signs of human activity in mangrove areas, as well. There, it has been suggested that deforestation and fragmentation in mangrove habitats have affected the local and nesting population of Roseate Spoonbills (*P. ajaja*) in the Guayaquil Gulf Estuary (Alava, 2005), as well as the declining population of the Brown Wood Rail (*A. wolfi*), which is endangered and less tolerant to habitat deterioration in Ecuador (Alava et al., 2007).

within the GMR if longlining occurs there (Anderson et al., 2003). In marine waters off northern Peru, thousands of waved albatrosses were estimated to be bycaught in smallscale longline fisheries (Jahncke et al., 2001). Mortality of adult albatrosses due to incidental and intentional (i.e., targeted fisheries for human consumption) in the artisanal Peruvian fishery possesses a serious threat for its conservation and remains as one of the stressors influencing the population dynamics of this species in recent years (Awkerman

Biological invasions are considered a leading cause of extinctions in terrestrial and marine ecosystem of marine protected areas (Boersma & Parrish, 1999; Bax et al., 2003). The introduction of exotic marine species and pathogens (viruses, bacteria and parasites) represents major threats for biodiversity and ecosystem functions, with potentially serious implications for fisheries resources, tourism, human health in marine protected areas and biosphere reserves (Carlton, 1989; Carlton & Geller, 1993; Carlton, 1996; Bax et al., 2003). Furthermore, emerging marine diseases in marine organisms have been linked to anthropogenic factors (Harvell et al., 1999). The Hawaiian Islands represents an extraordinary example of the negative effects of the biological invasion on endemic and native species (Vitousek et al., 1987). This is supported by the fact that Hawaii contains a large proportion of the imperilled USA endemic birds (43%) and plants (40%) threatened by alien species (Gurevitch & Padilla, 2004). The Galapagos Islands are facing a similar fate unless control and conservation strategies take place to mitigate biological invasion. Terrestrial invasive species, including mammalian predators and plants, significantly jeopardize native and endemic species inhabiting these remote islands (Snell et al., 2002).The number of registered introduced species in the archipelago has increased 10 times from 112 species in 1900 to 1321 in 2007 (Watkins & Cruz, 2007). Yet, this does not include introduced pathogens. Among the invasive pathogens, viruses, bacteria and parasites are the ones

Introduced plants including berries (*Rubus* spp.; black berry *Rubus niveus*) and quinine trees (*Cinchona pubescens*) have caused habitat loss and alteration for endemic species of birds such as the Galapagos Petrel and Galapagos Rail (Wiedenfeld & Jiménez-Uzcátegui, 2008). Introduced vertebrates are mainly predators affecting bird populations by killing many species of adult birds (cats *Felis catus*) and flightless or nesting species (dogs *Canis familiaris*  and pigs *Sus scrofa*); and by destroying nests and young (cats, dogs, black rat, *Rattus rattus*) (Jiménez-Uzcátegui & Wiedenfeld, 2002; Wiedenfeld & Jiménez-Uzcátegui, 2008). Some introduced viral diseases from domestic animals such as avian virus or avipoxvirus by domestic birds, fowlpox virus infecting chicken have threatened endemic species of birds (e.g., Darwin's finches) in the Galapagos (Wikelski et al., 2004). Thiel et al., (2005) has recently found presence of canarypox-like viruses in pox-like lesions of endemic passerine birds (Yellow Warblers, *Dendroica petechia*; finches, *Geospiza* spp.; and Galápagos mockingbirds, *Nesomimus parvulus*) from the inhabited islands of Santa Cruz and Isabela. A seroprevalence of 66% (29/44) to adenovirus group 1 has been found in waved albatrosses (*P. irrorata*) inhabiting Espanola Island (Padilla et al., 2003). Newcastle disease, Marek's disease virus (herpes) and mycoplasmosis detected in domestic chickens farmed on the islands (Vargas & Snell, 1997), has the potential to cause declines of the Flightless Cormorant (*P. harrisi*), Lava Gull (*L. fuliginosus*), and Galapagos Penguin (*S. mendiculus*), species with small population sizes. West Nile Virus (WNV) is expected to reach Ecuador

**5.3 Invasive species and emerging diseases: The Galapagos case** 

et al., 2006; Anderson et al., 2008).

possessing serious risk to the endemic fauna.

Fig. 4. Temporal and spatial evolution of mangroves, shrimp farming and salt flat areas (ha) on the continental coast of Ecuador from 1969 to 2006 (CLIRSEN, 2007).

#### **5.2 Fishery interactions**

Fishery bycatch, including longline fisheries, is categorized as the single major threat affecting many seabird populations and on the order of hundreds of thousands of seabirds, especially albatrosses, are caught and killed each year (BirdLife International, 2008; BirdLife International, 2009; Brothers et al., 2010). Industrial and artisanal fisheries, including commercial longline, gillnet and trawl fisheries, cause a significant mortality of seabirds (i.e., hundreds of thousands) each year around the global ocean, and in some cases, the effort of fishing activities (e.g., longline) overlaps with foraging grounds for seabirds (BirdLife International, 2008). Fishing activities outside of the boundaries (unprotected areas) of the Galapagos Marine Reserve possess a looming threat for seabirds such as albatrosses, petrels and shearwaters foraging frequently in these areas close to the continent (Jiménez-Uzcátegui & Wiedenfeld, 2002; Wiedenfeld & Jiménez-Uzcátegui 2008; Anderson et al., 2008). Among these, the waved albatross is probably the most affected seabird by fisheries interactions (e.g., longline fisheries) in the region. For instance, about 9-13 waved albatrosses were observed bycaught in longlines (i.e., 155 longline sets; 350 hooks per set) during a field study conducted with the artisanal fishing community of Santa Rosa in coastal Ecuador (Hardesty et al., 2010; J. Hardesty, pers. comm.). The bycatch incidence has been preliminary estimated in 0.11 albatrosses/1000 hooks, and most of the interactions are associated with artisanal longline fishing gears to capture hake (*Merluccius gayi*) (Arteaga et al., 2010). The bycatch assessment of pelagic longlining (High Seas Experimental Pilot Plan) conducted around water of the Galapagos Marine Reserve (GMR) in 2003 (Murillo et al., 2004) to evaluate the impact on epipelagic species and top predators did not report seabirds (e.g. albatrosses) as victims of bycatch, although it underscored the potential risk of bycatch for seabirds (Murillo et al., 2004). In contrast, a local artisanal tuna fishery, using single-hook lines with live sardines as bait within the GMR, reported catches up to five waved albatrosses per boat per day, indicating that a serious bycatch risk exists within the GMR if longlining occurs there (Anderson et al., 2003). In marine waters off northern Peru, thousands of waved albatrosses were estimated to be bycaught in smallscale longline fisheries (Jahncke et al., 2001). Mortality of adult albatrosses due to incidental and intentional (i.e., targeted fisheries for human consumption) in the artisanal Peruvian fishery possesses a serious threat for its conservation and remains as one of the stressors influencing the population dynamics of this species in recent years (Awkerman et al., 2006; Anderson et al., 2008).

#### **5.3 Invasive species and emerging diseases: The Galapagos case**

290 Ecosystems Biodiversity

**Mangrove Shrimp farms Salt flat areas**

**1969 1984 1987 1991 1995 1999 2006**

Fig. 4. Temporal and spatial evolution of mangroves, shrimp farming and salt flat areas (ha)

Fishery bycatch, including longline fisheries, is categorized as the single major threat affecting many seabird populations and on the order of hundreds of thousands of seabirds, especially albatrosses, are caught and killed each year (BirdLife International, 2008; BirdLife International, 2009; Brothers et al., 2010). Industrial and artisanal fisheries, including commercial longline, gillnet and trawl fisheries, cause a significant mortality of seabirds (i.e., hundreds of thousands) each year around the global ocean, and in some cases, the effort of fishing activities (e.g., longline) overlaps with foraging grounds for seabirds (BirdLife International, 2008). Fishing activities outside of the boundaries (unprotected areas) of the Galapagos Marine Reserve possess a looming threat for seabirds such as albatrosses, petrels and shearwaters foraging frequently in these areas close to the continent (Jiménez-Uzcátegui & Wiedenfeld, 2002; Wiedenfeld & Jiménez-Uzcátegui 2008; Anderson et al., 2008). Among these, the waved albatross is probably the most affected seabird by fisheries interactions (e.g., longline fisheries) in the region. For instance, about 9-13 waved albatrosses were observed bycaught in longlines (i.e., 155 longline sets; 350 hooks per set) during a field study conducted with the artisanal fishing community of Santa Rosa in coastal Ecuador (Hardesty et al., 2010; J. Hardesty, pers. comm.). The bycatch incidence has been preliminary estimated in 0.11 albatrosses/1000 hooks, and most of the interactions are associated with artisanal longline fishing gears to capture hake (*Merluccius gayi*) (Arteaga et al., 2010). The bycatch assessment of pelagic longlining (High Seas Experimental Pilot Plan) conducted around water of the Galapagos Marine Reserve (GMR) in 2003 (Murillo et al., 2004) to evaluate the impact on epipelagic species and top predators did not report seabirds (e.g. albatrosses) as victims of bycatch, although it underscored the potential risk of bycatch for seabirds (Murillo et al., 2004). In contrast, a local artisanal tuna fishery, using single-hook lines with live sardines as bait within the GMR, reported catches up to five waved albatrosses per boat per day, indicating that a serious bycatch risk exists

on the continental coast of Ecuador from 1969 to 2006 (CLIRSEN, 2007).

**0**

**5.2 Fishery interactions** 

**50,000**

**100,000**

**150,000**

**Area (ha)**

**200,000**

**250,000**

Biological invasions are considered a leading cause of extinctions in terrestrial and marine ecosystem of marine protected areas (Boersma & Parrish, 1999; Bax et al., 2003). The introduction of exotic marine species and pathogens (viruses, bacteria and parasites) represents major threats for biodiversity and ecosystem functions, with potentially serious implications for fisheries resources, tourism, human health in marine protected areas and biosphere reserves (Carlton, 1989; Carlton & Geller, 1993; Carlton, 1996; Bax et al., 2003). Furthermore, emerging marine diseases in marine organisms have been linked to anthropogenic factors (Harvell et al., 1999). The Hawaiian Islands represents an extraordinary example of the negative effects of the biological invasion on endemic and native species (Vitousek et al., 1987). This is supported by the fact that Hawaii contains a large proportion of the imperilled USA endemic birds (43%) and plants (40%) threatened by alien species (Gurevitch & Padilla, 2004). The Galapagos Islands are facing a similar fate unless control and conservation strategies take place to mitigate biological invasion. Terrestrial invasive species, including mammalian predators and plants, significantly jeopardize native and endemic species inhabiting these remote islands (Snell et al., 2002).The number of registered introduced species in the archipelago has increased 10 times from 112 species in 1900 to 1321 in 2007 (Watkins & Cruz, 2007). Yet, this does not include introduced pathogens. Among the invasive pathogens, viruses, bacteria and parasites are the ones possessing serious risk to the endemic fauna.

Introduced plants including berries (*Rubus* spp.; black berry *Rubus niveus*) and quinine trees (*Cinchona pubescens*) have caused habitat loss and alteration for endemic species of birds such as the Galapagos Petrel and Galapagos Rail (Wiedenfeld & Jiménez-Uzcátegui, 2008). Introduced vertebrates are mainly predators affecting bird populations by killing many species of adult birds (cats *Felis catus*) and flightless or nesting species (dogs *Canis familiaris*  and pigs *Sus scrofa*); and by destroying nests and young (cats, dogs, black rat, *Rattus rattus*) (Jiménez-Uzcátegui & Wiedenfeld, 2002; Wiedenfeld & Jiménez-Uzcátegui, 2008). Some introduced viral diseases from domestic animals such as avian virus or avipoxvirus by domestic birds, fowlpox virus infecting chicken have threatened endemic species of birds (e.g., Darwin's finches) in the Galapagos (Wikelski et al., 2004). Thiel et al., (2005) has recently found presence of canarypox-like viruses in pox-like lesions of endemic passerine birds (Yellow Warblers, *Dendroica petechia*; finches, *Geospiza* spp.; and Galápagos mockingbirds, *Nesomimus parvulus*) from the inhabited islands of Santa Cruz and Isabela. A seroprevalence of 66% (29/44) to adenovirus group 1 has been found in waved albatrosses (*P. irrorata*) inhabiting Espanola Island (Padilla et al., 2003). Newcastle disease, Marek's disease virus (herpes) and mycoplasmosis detected in domestic chickens farmed on the islands (Vargas & Snell, 1997), has the potential to cause declines of the Flightless Cormorant (*P. harrisi*), Lava Gull (*L. fuliginosus*), and Galapagos Penguin (*S. mendiculus*), species with small population sizes. West Nile Virus (WNV) is expected to reach Ecuador

(Solórzano, 1989). For example, banana plantations and agricultural lands use a broad spectrum of synthetic pesticides transported via run off and aerial dispersion to the estuaries and mangrove forests. However, the negative effects of chemical pollution on the coastal-estuarine environment have been scarcely characterized. The demand of pesticide usage for agricultural area is reflected by the importations of fungicides, insecticides and herbicides from January to May for both 2002 and 2003, with a total of 2,494 and 3,254 metric

The Salado Estuary, harboring the El Salado Mangrove–Wildlife Production Reserve, has been receiving about 60% from domestic use and 40% from industrial use, causing degradation of the water and sediment conditions of this estuary. Several studies from the Municipality of Guayaquil, National Fisheries Institute, and the Polytechnic School of the Litoral have reported low dissolved oxygen (DO) levels at the Salado Estuary, ranging from 0.74 mg/L to 2.4 mg/L, and pH as low as 5.7 over the surface sediment (Calle & Alava, 2009). A recent study on pollution by pesticides on the Taura River Basin, Gulf of Guayaquil, revealed the presence of several organochlorine (OC) and organophosphate (OP) and pyrethroid pesticides in samples of water, sediment and aquatic organisms (Montaño & Resabala, 2005). Some industrial and agricultural POPs such as PCBs and DDT were used in Ecuador after they were banned in the 1970s in developed countries, and therefore released to soil and water bodies. In continental Ecuador, DDT was applied inside houses (intradomiciliary applications) between 1957 and 1999 (Ministerio del Ambiente & ESPOL-ICQ , 2004), and a massive use of DDT was carried out during the 1980s to control the malaria vector-mosquito (Dr. Hugo Jurado, pers. comm.). The huge scale use of DDT culminated in 1988. At that time, however, DDT was also distributed without any control and used illegally for the agricultural sector to control crop pests (Dr. Hugo Jurado, pers. comm.). DDT was used, overused or misused, and therefore released to the soil and water bodies. To date, it has been pointed out that the only country still using DDT during the mid-1990 in South America was Ecuador; ironically, it was also the only country that experienced a significant decline in malaria (Mangu-Ward, 1997). DDT concentrations were reported on the Taura River Basin, Gulf of Guayaquil, in sediment (1.36 ug/kg wet weight) and aquatic organisms (2.87 ug/kg wet weight). The DDE/DDT ratio for these samples indicate relatively recent contamination by DDT-parental compound in sediment (ratio DDE/DDTs = 0.66) and fish (ratio DDE/DDTs=0.14) from the Taura River. The environmental implications and health effects of DDT use in aquatic birds and raptors is poorly understood and assessed in this country. The current levels, distribution, fate and effects of these POPs in environmental matrices (e.g.,

water, sediments, soil, fish and birds) have received scant attention.

Relatively high metal concentrations in sediment were reported for Hg (2.89 mg/kg dw), Pb (112 mg/kg dw), Cu (250 mg/kg dw), and Zn (550 mg/kg dw) exceeding the Effects Range Low (ERL) and the Effects Range Medium (ERM) sediment quality guidelines for Hg (0.71) and for Zn (410) (Calle & Alava, 2009). Organic (i.e., pesticides) and inorganic (metals) chemicals contaminants are a major problem not only for waterbirds, but for raptors associated to aquatic environments and several other species of wildlife. It is likely that individuals of Mangrove Black Hawk inhabiting mangroves close to commercial banana cultivation (i.e. the El Oro Province) might be facing exposures to chemicals and lethal effects both in the long and short terms (Alava et al., 2011), similar to that suggested for the Snail Kite (*Rosthramus sociabilis*) inhabiting and foraging in zones of vast rice fields and flooded areas of coastal Ecuador (e.g., Guayas, Los Rios and the El Oro provinces) where pesticides are broadly used (Alava et al., 2007). Ecotoxicological research is strongly

tonnes, respectively (SICA-MAG, 2003)

anytime and there is a high probability risk of its introduction into Galapagos unless strict control and preventive strategies are implemented prior to the arrival of the disease (GGEPL, 2004). The incidental transport of mosquitoes by boat or of infected vertebrate hosts is also significant risks for WNV invasion. If WNV is introduced in to Galapagos it is likely to cause catastrophic mortality of endemic birds, reptiles and mammals, leading to irreparable ecological and economic damage to the islands (GGEPL, 2004). The introduction of this disease is most likely to occur through the human transport of infectious mosquitoes, particularly via inadvertent transport in airplanes. Recently, several kinds of bacteria have already been detected in endemic sea bird and pinnipeds of the Galapagos. For example, while antibodies to avian adenovirus type 1 and *C. psittaci* were found in 31% (21/68) and 11% (7/65) of flightless cormorants, respectively, seventy-five of 84 (89%) Galapagos penguins had antibodies to *Chlamydophila psittaci,* but chlamydial DNA was not detected via polymerase chain reaction in samples from 30 birds (Travis et al., 2006a; Travis et al., 2006b). Waved albatrosses showed a seroprevalence of 9% (4/44) to avian encephalomyelitis; however, cloacal swabs were negative for *C. psittaci*-DNA. (Padilla et al., 2003). *Salmonella* sp. was reported in domestic pigeons (introduced rock doves, *Columba livia*) on San Cristóbal and may cause severe disease in species such as Galapagos doves (*Zenaida galapagoensis*) and other native birds (Harmon et al., 1987; Wikelski et al., 2004; Padilla et al., 2004). Among parasites, *Haemoproteus* sp., the only hemoparasite identified, was found in 89% of the Galapagos doves sampled but not in the rock doves (Padilla et al., 2004).

Currently, the major parasitic disease that could cause widespread mortality of native, endemic birds is the avian malaria, if it is introduced into Galapagos ecosystems. This parasite has caused severe mortality and decimation of a significant proportion of Hawaiian's endemic birds since it was introduced at beginning of 20th century (Wikelski et al., 2004). At present, despite its vector, the mosquito *Culex quinquefasciatus* (Diptera: Culicidae), is already established on the Galapagos Islands (Peck et al., 1998; Whiteman et al., 2005), there has been no report or detection of *Plasmodium relictum* (Wikelski *et al*. 2004; Thiel *et al*. 2005). A protozoan, *Trichomonas gallinae*, was reported in domestic pigeons (introduced rock doves, *Columba livia*) on San Cristóbal and may cause severe disease in species such as Galapagos doves (*Zenaida galapagoensis*) and other native birds (Harmon et al., 1987; Wikelski et al., 2004; Padilla et al., 2004). Because endemic species of birds of the Galapagos were not exposed to alien parasites transmitted by invasive species prior human occupation of the islands, they are more susceptible to the pathogenesis generated by parasitic diseases with potential risk at the population health level.

#### **5.4 Anthropogenic pollution**

Pollution coming from agriculture, forestry and industry significantly affects birds' population. Marine oil spills and persistent organic pollutants (POPs) can have a significant impact on population of seabirds (BirdLife International, 2008a). In Ecuador, the Guayaquil Gulf Estuary Basin has become the sink receiving point and non point sources of contamination over the last 80 years. As agriculture is the fundamental base for the Ecuador economic activity, the predominant crops are banana plantation, rice fields, sugar cane and cocoa in the Gulf of Guayaquil. In 2005, the total land used/harvest area for banana, coffee, rice, maize and cocoa ranged from 1,269,775 to 1,652,600 ha (INEC, 2007; FAO, 2007). In the past, farmers conducted both extensive and intensive use and application of fertilizers, herbicides and pesticides, including some organochlorine pollutants banned in others countries such as DDTs, chlordanes, heptachlor, dieldrin, aldrin, mirex, and lindane

anytime and there is a high probability risk of its introduction into Galapagos unless strict control and preventive strategies are implemented prior to the arrival of the disease (GGEPL, 2004). The incidental transport of mosquitoes by boat or of infected vertebrate hosts is also significant risks for WNV invasion. If WNV is introduced in to Galapagos it is likely to cause catastrophic mortality of endemic birds, reptiles and mammals, leading to irreparable ecological and economic damage to the islands (GGEPL, 2004). The introduction of this disease is most likely to occur through the human transport of infectious mosquitoes, particularly via inadvertent transport in airplanes. Recently, several kinds of bacteria have already been detected in endemic sea bird and pinnipeds of the Galapagos. For example, while antibodies to avian adenovirus type 1 and *C. psittaci* were found in 31% (21/68) and 11% (7/65) of flightless cormorants, respectively, seventy-five of 84 (89%) Galapagos penguins had antibodies to *Chlamydophila psittaci,* but chlamydial DNA was not detected via polymerase chain reaction in samples from 30 birds (Travis et al., 2006a; Travis et al., 2006b). Waved albatrosses showed a seroprevalence of 9% (4/44) to avian encephalomyelitis; however, cloacal swabs were negative for *C. psittaci*-DNA. (Padilla et al., 2003). *Salmonella* sp. was reported in domestic pigeons (introduced rock doves, *Columba livia*) on San Cristóbal and may cause severe disease in species such as Galapagos doves (*Zenaida galapagoensis*) and other native birds (Harmon et al., 1987; Wikelski et al., 2004; Padilla et al., 2004). Among parasites, *Haemoproteus* sp., the only hemoparasite identified, was found in

89% of the Galapagos doves sampled but not in the rock doves (Padilla et al., 2004).

parasitic diseases with potential risk at the population health level.

**5.4 Anthropogenic pollution** 

Currently, the major parasitic disease that could cause widespread mortality of native, endemic birds is the avian malaria, if it is introduced into Galapagos ecosystems. This parasite has caused severe mortality and decimation of a significant proportion of Hawaiian's endemic birds since it was introduced at beginning of 20th century (Wikelski et al., 2004). At present, despite its vector, the mosquito *Culex quinquefasciatus* (Diptera: Culicidae), is already established on the Galapagos Islands (Peck et al., 1998; Whiteman et al., 2005), there has been no report or detection of *Plasmodium relictum* (Wikelski *et al*. 2004; Thiel *et al*. 2005). A protozoan, *Trichomonas gallinae*, was reported in domestic pigeons (introduced rock doves, *Columba livia*) on San Cristóbal and may cause severe disease in species such as Galapagos doves (*Zenaida galapagoensis*) and other native birds (Harmon et al., 1987; Wikelski et al., 2004; Padilla et al., 2004). Because endemic species of birds of the Galapagos were not exposed to alien parasites transmitted by invasive species prior human occupation of the islands, they are more susceptible to the pathogenesis generated by

Pollution coming from agriculture, forestry and industry significantly affects birds' population. Marine oil spills and persistent organic pollutants (POPs) can have a significant impact on population of seabirds (BirdLife International, 2008a). In Ecuador, the Guayaquil Gulf Estuary Basin has become the sink receiving point and non point sources of contamination over the last 80 years. As agriculture is the fundamental base for the Ecuador economic activity, the predominant crops are banana plantation, rice fields, sugar cane and cocoa in the Gulf of Guayaquil. In 2005, the total land used/harvest area for banana, coffee, rice, maize and cocoa ranged from 1,269,775 to 1,652,600 ha (INEC, 2007; FAO, 2007). In the past, farmers conducted both extensive and intensive use and application of fertilizers, herbicides and pesticides, including some organochlorine pollutants banned in others countries such as DDTs, chlordanes, heptachlor, dieldrin, aldrin, mirex, and lindane (Solórzano, 1989). For example, banana plantations and agricultural lands use a broad spectrum of synthetic pesticides transported via run off and aerial dispersion to the estuaries and mangrove forests. However, the negative effects of chemical pollution on the coastal-estuarine environment have been scarcely characterized. The demand of pesticide usage for agricultural area is reflected by the importations of fungicides, insecticides and herbicides from January to May for both 2002 and 2003, with a total of 2,494 and 3,254 metric tonnes, respectively (SICA-MAG, 2003)

The Salado Estuary, harboring the El Salado Mangrove–Wildlife Production Reserve, has been receiving about 60% from domestic use and 40% from industrial use, causing degradation of the water and sediment conditions of this estuary. Several studies from the Municipality of Guayaquil, National Fisheries Institute, and the Polytechnic School of the Litoral have reported low dissolved oxygen (DO) levels at the Salado Estuary, ranging from 0.74 mg/L to 2.4 mg/L, and pH as low as 5.7 over the surface sediment (Calle & Alava, 2009). A recent study on pollution by pesticides on the Taura River Basin, Gulf of Guayaquil, revealed the presence of several organochlorine (OC) and organophosphate (OP) and pyrethroid pesticides in samples of water, sediment and aquatic organisms (Montaño & Resabala, 2005). Some industrial and agricultural POPs such as PCBs and DDT were used in Ecuador after they were banned in the 1970s in developed countries, and therefore released to soil and water bodies. In continental Ecuador, DDT was applied inside houses (intradomiciliary applications) between 1957 and 1999 (Ministerio del Ambiente & ESPOL-ICQ , 2004), and a massive use of DDT was carried out during the 1980s to control the malaria vector-mosquito (Dr. Hugo Jurado, pers. comm.). The huge scale use of DDT culminated in 1988. At that time, however, DDT was also distributed without any control and used illegally for the agricultural sector to control crop pests (Dr. Hugo Jurado, pers. comm.). DDT was used, overused or misused, and therefore released to the soil and water bodies. To date, it has been pointed out that the only country still using DDT during the mid-1990 in South America was Ecuador; ironically, it was also the only country that experienced a significant decline in malaria (Mangu-Ward, 1997). DDT concentrations were reported on the Taura River Basin, Gulf of Guayaquil, in sediment (1.36 ug/kg wet weight) and aquatic organisms (2.87 ug/kg wet weight). The DDE/DDT ratio for these samples indicate relatively recent contamination by DDT-parental compound in sediment (ratio DDE/DDTs = 0.66) and fish (ratio DDE/DDTs=0.14) from the Taura River. The environmental implications and health effects of DDT use in aquatic birds and raptors is poorly understood and assessed in this country. The current levels, distribution, fate and effects of these POPs in environmental matrices (e.g., water, sediments, soil, fish and birds) have received scant attention.

Relatively high metal concentrations in sediment were reported for Hg (2.89 mg/kg dw), Pb (112 mg/kg dw), Cu (250 mg/kg dw), and Zn (550 mg/kg dw) exceeding the Effects Range Low (ERL) and the Effects Range Medium (ERM) sediment quality guidelines for Hg (0.71) and for Zn (410) (Calle & Alava, 2009). Organic (i.e., pesticides) and inorganic (metals) chemicals contaminants are a major problem not only for waterbirds, but for raptors associated to aquatic environments and several other species of wildlife. It is likely that individuals of Mangrove Black Hawk inhabiting mangroves close to commercial banana cultivation (i.e. the El Oro Province) might be facing exposures to chemicals and lethal effects both in the long and short terms (Alava et al., 2011), similar to that suggested for the Snail Kite (*Rosthramus sociabilis*) inhabiting and foraging in zones of vast rice fields and flooded areas of coastal Ecuador (e.g., Guayas, Los Rios and the El Oro provinces) where pesticides are broadly used (Alava et al., 2007). Ecotoxicological research is strongly

Increasing emissions of greenhouse gases, including carbon dioxide (CO2) due to fossil fuel, and increases in global average air and ocean temperatures are the major forces driving global warming in the last century and in recent times (IPCC, 2007). A warming (global surface temperature) of about 0.2 °C per decade is projected for the next two decades according to scenarios of the Intergovernmental Panel on Climate Change (IPPC, 2007). Warming is larger in the Western Equatorial Pacific than in the Eastern Equatorial Pacific over the past century, suggesting that the increased West-East temperature gradient may have increased the likelihood of strong El Niños, such as those of 1983 and 1998 (Timmermann et al., 1999; Hansen et al., 2006). It has been predicted that anthropogenic warming and sea level rise would continue for centuries due to the time scales associated with climate processes and feedbacks, even if greenhouse gas concentrations were to be stabilized (IPPC, 2007). Global warming of more than ≈1°C, relative to 2000, will constitute dangerous climate change due to

Seabirds are key indicators of the impact of climate change on the global ocean (BirdLife International, 2008b). Although the impact of climate change on several large-scale oceanoclimatic fluctuations, including the El Niño-Southern Oscillation, (ENSO) is difficult to predict, it has been suggested that global warming may result in more frequent and intense

Fig. 5. Time series data of Galapagos penguin (grey bars) and Flightless cormorant (white bars) populations and sea surface temperature (SST) anomalies (dashed line) for El Niño regions 1 and 2, which engulf the Galapagos Archipelago in the Southeastern Tropical Pacific Ocean region. The positive temperature anomalies exceeding 2°C (solid, black line) indicate strong El Niño events (i.e., 1982-1983; and, 1997-1998). SST anomalies are good indicator of El Niño events; thus, SST anomaly data was collected between 1969 and 2009. SST anomalies were available from the NOAA National Weather Service (NOAA, 2011): (http://www.cpc.ncep.noaa.gov/products/analysis\_monitoring/ensostuff/ONI\_change.

**-1.5**

**-1**

**-0.5**

**0**

**0.5**

**Sea Surface Temperature Anomaly (°C)**

**1**

**1.5**

**2**

**2.5**

**3**

**Galapagos penguin Flightless cormorant SST anomaly**

likely effects on sea level and extinction of species (Hansen et al., 2006).

**5.5 Regional climate variability** 

**0 200 400 600 800 1,000 1,200 1,400 1,600 1,800 2,000 2,200**

shtml).

**Population** 

encouraged in Ecuador to determine the levels, food web bioaccumulation and effects of insecticides and herbicides (e.g., organochlorines, organophosphates, carbamates, bipiridyls) in top predator birds, including water birds and raptors.

Marine pollution by debris in Galapagos waters is emerging as a significant concern for biota. A beach-shoreline cleanup program around the Galapagos in 1999 retrieved 22,140 kg of debris, with plastics and metals being the predominant objects at 25 and 28% of the total (Fundación Natura & WWF 2000; Alava, 2011). At sea, the accidental or deliberate disposal of solid waste (e. g., plastic, fishery gear) from both tourism and fishing vessels represent a threat for marine vertebrates such as large pelagic fish, sea turtles, cetaceans, sea lions, fur seals and sea birds (Alava, 2011). Likewise, both intentional (operational) and unintentional (accidental) fuel and oil releases occur around the islands from ships, with the former occurring in the long-term causing chronic degradation and latter resulting in acute impacts to the marine environment (Lessmann, 2004). Oil spills offer perhaps the most visible example of pollutant impacts on sea life. During the last two decades, several oil spills have taken place in the Galapagos (Table 4). A major oil spill that threatened a significant part of the GMR was the *MV Jessica* spill on 16 January 2001 at the entrance of Naufragio Bay (89 37'15"W, 053'40"S), San Cristóbal Island. The oil tanker released almost 100% of its total cargo consisting of 302,824 L of IFO 120–bunker fuel (Fuel Oil 120) and 605,648 L of Diesel oil # 2 (DO#2) (Lougheed et al., 2002; Edgar et al., 2003). Although no oiled seabirds were recorded at the time of this oil spill (Lougheed et al., 2002), researcher doing field work in Española Island found five oiled Nazca boobies (*Sula granti*) in January 2001, one oiled waved albatross in June 2001, and two oiled Nazca boobies in November 2001, confirming that these birds were polluted by spilled oil (Anderson et al., 2003). In early July 2002, a second oil spill took place in the Galapagos, when a small tanker (*BAE/Taurus*) sank and spilled diesel fuel in waters off the coast of Puerto Villamil, Isabela Island. Fortunately, no sign of fuel was found on the beaches or on marine animals (including sea birds), due to mitigation efforts conducted by the GNPS and Charles Darwin Foundation. Other low magnitude oil spill events have also occurred (Lessmann, 2004). The chronic toxic effects of the 2001−Jessica oil spill's residues on unique vulnerable population of Galapagos marine iguanas (*Amblyrhynchus cristatus*) has been well documented elsewhere (Wikelski et al., 2001; Wikelski et al., 2002). Less visible and more insidious global toxicants of concern involve POPs (i.e., PCBs, DDTs and several other organochlorine pesticides), which have recently been detected and assessed in fish collected from Galapagos waters and in Galapagos sea lions (*Zalophus wollebaeki*) (Alava et al., 2009; Alava et al., 2011; Alava, 2011), but these contaminants still need to be investigated in seabirds endemic to the Galapagos.


Table 4. Inventory of oil and diesel spills in the Galapagos from 2001 to 2006. \*151,412 L of fuel were estimated to be contained in the boat, but actual volume spilled was not reported (adapted from Alava, 2001).

#### **5.5 Regional climate variability**

294 Ecosystems Biodiversity

encouraged in Ecuador to determine the levels, food web bioaccumulation and effects of insecticides and herbicides (e.g., organochlorines, organophosphates, carbamates, bipiridyls)

Marine pollution by debris in Galapagos waters is emerging as a significant concern for biota. A beach-shoreline cleanup program around the Galapagos in 1999 retrieved 22,140 kg of debris, with plastics and metals being the predominant objects at 25 and 28% of the total (Fundación Natura & WWF 2000; Alava, 2011). At sea, the accidental or deliberate disposal of solid waste (e. g., plastic, fishery gear) from both tourism and fishing vessels represent a threat for marine vertebrates such as large pelagic fish, sea turtles, cetaceans, sea lions, fur seals and sea birds (Alava, 2011). Likewise, both intentional (operational) and unintentional (accidental) fuel and oil releases occur around the islands from ships, with the former occurring in the long-term causing chronic degradation and latter resulting in acute impacts to the marine environment (Lessmann, 2004). Oil spills offer perhaps the most visible example of pollutant impacts on sea life. During the last two decades, several oil spills have taken place in the Galapagos (Table 4). A major oil spill that threatened a significant part of the GMR was the *MV Jessica* spill on 16 January 2001 at the entrance of Naufragio Bay (89 37'15"W, 053'40"S), San Cristóbal Island. The oil tanker released almost 100% of its total cargo consisting of 302,824 L of IFO 120–bunker fuel (Fuel Oil 120) and 605,648 L of Diesel oil # 2 (DO#2) (Lougheed et al., 2002; Edgar et al., 2003). Although no oiled seabirds were recorded at the time of this oil spill (Lougheed et al., 2002), researcher doing field work in Española Island found five oiled Nazca boobies (*Sula granti*) in January 2001, one oiled waved albatross in June 2001, and two oiled Nazca boobies in November 2001, confirming that these birds were polluted by spilled oil (Anderson et al., 2003). In early July 2002, a second oil spill took place in the Galapagos, when a small tanker (*BAE/Taurus*) sank and spilled diesel fuel in waters off the coast of Puerto Villamil, Isabela Island. Fortunately, no sign of fuel was found on the beaches or on marine animals (including sea birds), due to mitigation efforts conducted by the GNPS and Charles Darwin Foundation. Other low magnitude oil spill events have also occurred (Lessmann, 2004). The chronic toxic effects of the 2001−Jessica oil spill's residues on unique vulnerable population of Galapagos marine iguanas (*Amblyrhynchus cristatus*) has been well documented elsewhere (Wikelski et al., 2001; Wikelski et al., 2002). Less visible and more insidious global toxicants of concern involve POPs (i.e., PCBs, DDTs and several other organochlorine pesticides), which have recently been detected and assessed in fish collected from Galapagos waters and in Galapagos sea lions (*Zalophus wollebaeki*) (Alava et al., 2009; Alava et al., 2011; Alava, 2011), but these contaminants still need to be investigated in seabirds endemic to the Galapagos.

**Boat/Tanker Date Site Quantity** 

*Motor Yacht Iguana* June 1988 Santa Cruz Island 189,265 *MV/Jessica* 16 January 2001 Naufragio Bay, San Cristóbal 908,472 *BAE/Taurus* 4-7 July 2002 Puerto Villamil, Isabela Island 7571

Table 4. Inventory of oil and diesel spills in the Galapagos from 2001 to 2006. \*151,412 L of fuel were estimated to be contained in the boat, but actual volume spilled was not reported

Academia Bay, Puerto Ayora,

Santa Cruz Island

13-14 September

2005

*MV/Galapagos-Explorer* 

(adapted from Alava, 2001).

**(L)** 

Not reported\*

in top predator birds, including water birds and raptors.

Increasing emissions of greenhouse gases, including carbon dioxide (CO2) due to fossil fuel, and increases in global average air and ocean temperatures are the major forces driving global warming in the last century and in recent times (IPCC, 2007). A warming (global surface temperature) of about 0.2 °C per decade is projected for the next two decades according to scenarios of the Intergovernmental Panel on Climate Change (IPPC, 2007). Warming is larger in the Western Equatorial Pacific than in the Eastern Equatorial Pacific over the past century, suggesting that the increased West-East temperature gradient may have increased the likelihood of strong El Niños, such as those of 1983 and 1998 (Timmermann et al., 1999; Hansen et al., 2006). It has been predicted that anthropogenic warming and sea level rise would continue for centuries due to the time scales associated with climate processes and feedbacks, even if greenhouse gas concentrations were to be stabilized (IPPC, 2007). Global warming of more than ≈1°C, relative to 2000, will constitute dangerous climate change due to likely effects on sea level and extinction of species (Hansen et al., 2006).

Seabirds are key indicators of the impact of climate change on the global ocean (BirdLife International, 2008b). Although the impact of climate change on several large-scale oceanoclimatic fluctuations, including the El Niño-Southern Oscillation, (ENSO) is difficult to predict, it has been suggested that global warming may result in more frequent and intense

Fig. 5. Time series data of Galapagos penguin (grey bars) and Flightless cormorant (white bars) populations and sea surface temperature (SST) anomalies (dashed line) for El Niño regions 1 and 2, which engulf the Galapagos Archipelago in the Southeastern Tropical Pacific Ocean region. The positive temperature anomalies exceeding 2°C (solid, black line) indicate strong El Niño events (i.e., 1982-1983; and, 1997-1998). SST anomalies are good indicator of El Niño events; thus, SST anomaly data was collected between 1969 and 2009. SST anomalies were available from the NOAA National Weather Service (NOAA, 2011): (http://www.cpc.ncep.noaa.gov/products/analysis\_monitoring/ensostuff/ONI\_change. shtml).

2011b). Some of the species include the Western Sandpiper (*C. mauri*), Semipalmated Sandpiper (*C. pusilla*) and Sanderling (*C. alba*). The decline is more evident after the El Niño

Several international conventions aimed to conserve and protect the biodiversity and environment as well as cultural and natural heritage within the country have been signed and ratified by the Ecuadorian government. These include the Convention on Biological Diversity (CBD, ratified in 1993), World Heritage Convention (signed in 1973), Convention on Migratory species (ratified in 2004), Convention on International Trade in Endangered Species of Wild Fauna and Flora (signed in 1974), Ramsar Convention on Wetlands (ratified in 1990). Ecuador has also signed bilateral environmental agreements with Peru and Colombia. Despite of Ecuador's commitment to internalize and pursue the goals of these agreements and the existence of several environmental laws, regulations and acts at the National level, lack of law empowering is observed at the local and regional levels and violations are scarcely sanctioned. Empowerment and enforcement of regulations and laws are necessary to accomplish legal protection of threatened species and conservation of critical habitats for waterbirds. Best management practices and effective land-use zoning, utilizing buffer zones between agricultural (plantations and farms) areas and the mangrove wetlands would ensure protection of local biodiversity. Best framing practices and the establishment of buffer zones (i.e., 100m) are needed to mitigate the agriculture expansion and cattle ranching in some areas such as those found around the El Canclon lagoon and Santay Island. Community-based conservation and environmental awareness might be undertaken by building capacity of local stakeholders (e.g. farmers and ranchers) in sustainable aquaculture/agriculture and nature tourism in areas that have received scant attention. At the Ecuasal lagoons, for instance, the owner and manager (Ecuasal Company) of the two production plants (Salinas and Pacoa lagoons) has lent its facilities to local ornithologists for the study of the birds and has shown great interest in supporting bird conservation and ecotourism during the last 10 years. Likewise, the Control and Surveillance System of the Mangrove Clear-Cutting Project conducted by Fundacion Natura and the National Chamber of Aquaculture hampered significantly the deforestation of mangrove forests on the Ecuadorian continental coast between 1998 and 2002 (Carvajal & Alava, 2007). Yet, field research is necessary for studying the relationship between the abundance waterbird species, including common and rare

Introduced plants and animals represent one of the greatest threats to the ecosystems of Galapagos**.** The invasive species eradication and control program of the Galapagos National Park Service and the Galapagos Inspection and Quarantine System (SICGAL) promise the avoidance and restriction of alien species to the islands. A recent triumph in this arena was the successful eradication of introduced and feral goats in Santiago Island (Cruz et al., 2009); yet, goats from other island still need to be removed. Similarly, industrial longline fishing activities have continued within Galapagos waters and several illegal vessels have been confiscated since the GMR was established. It has been suggested that the reduction of adult mortality of albatrosses in the coastal fishery of Ecuador and Peru appears to be the most effective means to stabilize this threatened species (Anderson et al., 2008). Currently, the ongoing institutional cooperation and surveillance system involving the Galapagos National Park Service, The Ecuadorian Navy Forces and non-governmental organizations assure in

event of 1997-1998 (Haase, 2011b), as shown in Fig. 6.

**6. Conservation and management implications** 

species, and disturbed and undisturbed mangrove areas.

El Niño events (Timmermann et al., 1999). Therefore, it is likely that the most significant threat from global climate change is its potential to affect the frequency and severity of ENSO events and the associated to lack of primary productivity, impacting endemic Galapagos seabirds and coastal waterbirds (Vargas et al., 2006; Wiedenfeld & Jiménez-Uzcátegui, 2008). Increases in sea surface temperature deplete primary production disrupting the bottom of marine food webs, and therefore top predators. El Niño may severely affect marine species especially small population of seabird such Galapagos penguins and Flightless cormorants (Wiedenfeld & Jiménez-Uzcátegui, 2008; Vargas et al., 2006). For instance, the 2004 penguin population (858 penguins) was estimated to be less than 50% of that prior to the strongest 1982–1983 El Niño event, including the population counted in the early 1970s, when the total number was 1931 penguins (Vargas et al., 2005; Vargas et al., 2006; Vargas et al., 2007), as shown in Fig 5. This underlines that the strong El Niño events of 1982-1983 and 1997-1998 were followed by population declines of more than 60% from which the species has yet to recover (Vargas et al., 2007). The censuses for Galapagos penguin and Flightless cormorants conducted in the last decade (2000-2010) appear to show a moderate positive or stable trend for both species (Jiménez-Uzcátegui et al., 2006; Jiménez-Uzcátegui & Vargas, 2007; Jiménez-Uzcátegui & Devineau, 2009), underscoring the potential recover during cold La Niña episodes (Vargas et al., 2006), but above all the ecological resilience of these endemic seabirds to overcome the environmental change and. In addition, sea level rise and shift in suitable climatic conditions attributable to global warming may damage coastal habitats such as mangroves and lagoons (Wiedenfeld & Jiménez-Uzcátegui, 2008; BirdLife International, 2008b).

Fig. 6. Local population trends of migratory sandpipers observed at Ecuasal lagoons on coastal Ecuador from 1990 to 2011 (data adapted from Haase, 2011b).

Similarly, negative trends have recently been observed for local populations of several migratory shorebird species overwintering at coastal Ecuador from 1991 to 2011 (Haase, 2011b). Some of the species include the Western Sandpiper (*C. mauri*), Semipalmated Sandpiper (*C. pusilla*) and Sanderling (*C. alba*). The decline is more evident after the El Niño event of 1997-1998 (Haase, 2011b), as shown in Fig. 6.

## **6. Conservation and management implications**

296 Ecosystems Biodiversity

El Niño events (Timmermann et al., 1999). Therefore, it is likely that the most significant threat from global climate change is its potential to affect the frequency and severity of ENSO events and the associated to lack of primary productivity, impacting endemic Galapagos seabirds and coastal waterbirds (Vargas et al., 2006; Wiedenfeld & Jiménez-Uzcátegui, 2008). Increases in sea surface temperature deplete primary production disrupting the bottom of marine food webs, and therefore top predators. El Niño may severely affect marine species especially small population of seabird such Galapagos penguins and Flightless cormorants (Wiedenfeld & Jiménez-Uzcátegui, 2008; Vargas et al., 2006). For instance, the 2004 penguin population (858 penguins) was estimated to be less than 50% of that prior to the strongest 1982–1983 El Niño event, including the population counted in the early 1970s, when the total number was 1931 penguins (Vargas et al., 2005; Vargas et al., 2006; Vargas et al., 2007), as shown in Fig 5. This underlines that the strong El Niño events of 1982-1983 and 1997-1998 were followed by population declines of more than 60% from which the species has yet to recover (Vargas et al., 2007). The censuses for Galapagos penguin and Flightless cormorants conducted in the last decade (2000-2010) appear to show a moderate positive or stable trend for both species (Jiménez-Uzcátegui et al., 2006; Jiménez-Uzcátegui & Vargas, 2007; Jiménez-Uzcátegui & Devineau, 2009), underscoring the potential recover during cold La Niña episodes (Vargas et al., 2006), but above all the ecological resilience of these endemic seabirds to overcome the environmental change and. In addition, sea level rise and shift in suitable climatic conditions attributable to global warming may damage coastal habitats such as mangroves and lagoons (Wiedenfeld

> **Semipalmated Sandpiper Western Sanpiper Sanderling**

& Jiménez-Uzcátegui, 2008; BirdLife International, 2008b).

1997-1998 ENSO event

Fig. 6. Local population trends of migratory sandpipers observed at Ecuasal lagoons on

Similarly, negative trends have recently been observed for local populations of several migratory shorebird species overwintering at coastal Ecuador from 1991 to 2011 (Haase,

coastal Ecuador from 1990 to 2011 (data adapted from Haase, 2011b).

**0.00**

**2,000.00**

**4,000.00**

**6,000.00**

**Overwintering Population**

**8,000.00**

**10,000.00**

**12,000.00**

Several international conventions aimed to conserve and protect the biodiversity and environment as well as cultural and natural heritage within the country have been signed and ratified by the Ecuadorian government. These include the Convention on Biological Diversity (CBD, ratified in 1993), World Heritage Convention (signed in 1973), Convention on Migratory species (ratified in 2004), Convention on International Trade in Endangered Species of Wild Fauna and Flora (signed in 1974), Ramsar Convention on Wetlands (ratified in 1990). Ecuador has also signed bilateral environmental agreements with Peru and Colombia. Despite of Ecuador's commitment to internalize and pursue the goals of these agreements and the existence of several environmental laws, regulations and acts at the National level, lack of law empowering is observed at the local and regional levels and violations are scarcely sanctioned. Empowerment and enforcement of regulations and laws are necessary to accomplish legal protection of threatened species and conservation of critical habitats for waterbirds. Best management practices and effective land-use zoning, utilizing buffer zones between agricultural (plantations and farms) areas and the mangrove wetlands would ensure protection of local biodiversity. Best framing practices and the establishment of buffer zones (i.e., 100m) are needed to mitigate the agriculture expansion and cattle ranching in some areas such as those found around the El Canclon lagoon and Santay Island. Community-based conservation and environmental awareness might be undertaken by building capacity of local stakeholders (e.g. farmers and ranchers) in sustainable aquaculture/agriculture and nature tourism in areas that have received scant attention. At the Ecuasal lagoons, for instance, the owner and manager (Ecuasal Company) of the two production plants (Salinas and Pacoa lagoons) has lent its facilities to local ornithologists for the study of the birds and has shown great interest in supporting bird conservation and ecotourism during the last 10 years. Likewise, the Control and Surveillance System of the Mangrove Clear-Cutting Project conducted by Fundacion Natura and the National Chamber of Aquaculture hampered significantly the deforestation of mangrove forests on the Ecuadorian continental coast between 1998 and 2002 (Carvajal & Alava, 2007). Yet, field research is necessary for studying the relationship between the abundance waterbird species, including common and rare species, and disturbed and undisturbed mangrove areas.

Introduced plants and animals represent one of the greatest threats to the ecosystems of Galapagos**.** The invasive species eradication and control program of the Galapagos National Park Service and the Galapagos Inspection and Quarantine System (SICGAL) promise the avoidance and restriction of alien species to the islands. A recent triumph in this arena was the successful eradication of introduced and feral goats in Santiago Island (Cruz et al., 2009); yet, goats from other island still need to be removed. Similarly, industrial longline fishing activities have continued within Galapagos waters and several illegal vessels have been confiscated since the GMR was established. It has been suggested that the reduction of adult mortality of albatrosses in the coastal fishery of Ecuador and Peru appears to be the most effective means to stabilize this threatened species (Anderson et al., 2008). Currently, the ongoing institutional cooperation and surveillance system involving the Galapagos National Park Service, The Ecuadorian Navy Forces and non-governmental organizations assure in

**conservation status**

Rare/Accidental/**Near-**

**threatened**

**endangered**

Order: Family/common name Species Remarks/**Global** 

Great Grebe *Podiceps major* Rare/Accidental Silvery Grebe *Podiceps occipitalis* **Least Concern** 

Chilean Flamingo *Phoenicopterus chilensis* **Near-threatened** 

Black-browed Albatross *Thalassarche melanophris* Rare/Accidental Wandering Albatross *Diomedea exulans* Rare/Accidental Waved Albatross *Phoebastria irrorata* **Critically endangered** 

Southern Fulmar *Fulmarus glacialoides* Rare/Accidental Cape Petrel *Daption capense* Rare/Accidental

Gould's Petrel *Pterodroma leucoptera* Rare/Accidental

Wilson's Storm-Petrel *Oceanites oceanicus* Rare/Accidental Elliot's Storm-Petrel *Oceanites gracilis* Data deficient White-faced Storm-Petrel *Pelagodroma marina* Rare/Accidental White-bellied Storm-Petrel *Fregetta grallaria* Rare/Accidental Polynesian Storm-Petrel *Nesofregetta fuliginosa* Vulnerable

Leach's Storm-Petrel *Oceanodroma leucorhoa* Rare/Accidental

Wedge-tailed Shearwater *Puffinus pacificus* Rare

Parkinson's Petrel *Procellaria parkinsoni* **Common/Vulnerable**  Pink-footed Shearwater *Puffinus creatopus* Accidental/**Vulnerable**

Humboldt Penguin *Spheniscus humboldti* Rare/Accidental/**Vulnerable** Galapagos Penguin *Spheniscus mendiculus* Endemic/ **Endangered**

Black-footed Albatross *Phoebastria nigripes* Rare/Accidental/**Endangered**

Galapagos Petrel *Pterodroma phaeopygia* Breeding endemic/**Critically** 

White-chinned Petrel *Procellaria aequinoctialis* Rare/Accidental/**Vulnerable**

Buller's Shearwater *Puffinus bulleri* Rare/Accidental/**Vulnerable** Sooty Shearwater *Puffinus griseus* Near-threatened; Common Galapagos Shearwater *Puffinus subalaris* Endemic/Rare coastal

Ringed Storm-Petrel *Oceanodroma hornbyi* Accidental/**Data deficient**

Pied-billed Grebe *Podilymbus podiceps* 

American Flamingo *Phoenicopterus ruber* 

Southern Giant-Petrel *Macronectes giganteus* 

PHOENICOPTERIFORMES:

Phoenicopteridae

Spheniscidae

Diomedeidae

Procellariidae

SPHENISCIFORMES:

PROCELLARIIFORMES:

PROCELLARIIFORMES:

PROCELLARIIFORMES:

Hydrobatidae

somehow the control and enforcement of fishing prohibitions to mitigate the bycatch problem within the GMR.

#### **7. Acknowledgements**

We acknowledge the field work by volunteers and our assistants, M. Constantino, E. Astudillo, X. Arosemena, A. Martinez, M. Peñafiel and C. Bohórquez, C. Gutierrez, G. Nazareno, M. Bruno, G. Baez, P. J. Jimenez, R. Carvajal and C. Cajas as well as the volunteers of the Ecuadorian Foundation for the Study of Marine Mammals. Part of the information and data generated for this contribution was possible under the project 'Conservation of the El Canclon Lake to protect *Anhima cornuta* in the Manglares Churute National Ecological Reserve (ECU/00/009), awarded by the GEF–Small Grant Programme (Operational programme OP2: Coastal, Marine and Freshwater Ecosystems) of the United Nations Development Programm, as well as the Project, Control and Surveillance System of the Mangrove Clear-Cutting on the Ecuadorian Continental Coast sponsored by the National Chamber of Aquaculture (Camara Nacional de Acuacultura). Both projects were administered by Fundación Natura Capítulo. We are greatful to the Ecuasal Company, for giving permission to do the census and field work within their property. The census work and the banding project were carried out with financial help from the US Fish and Wildlife Service, the Canadian Wildlife service and the Manomet Centre for conservation Sciences. Special thanks to Brian Harrington, Robert Elner and Ron Ydenberg for stimulating our conservation efforts in Ecuador.


somehow the control and enforcement of fishing prohibitions to mitigate the bycatch

We acknowledge the field work by volunteers and our assistants, M. Constantino, E. Astudillo, X. Arosemena, A. Martinez, M. Peñafiel and C. Bohórquez, C. Gutierrez, G. Nazareno, M. Bruno, G. Baez, P. J. Jimenez, R. Carvajal and C. Cajas as well as the volunteers of the Ecuadorian Foundation for the Study of Marine Mammals. Part of the information and data generated for this contribution was possible under the project 'Conservation of the El Canclon Lake to protect *Anhima cornuta* in the Manglares Churute National Ecological Reserve (ECU/00/009), awarded by the GEF–Small Grant Programme (Operational programme OP2: Coastal, Marine and Freshwater Ecosystems) of the United Nations Development Programm, as well as the Project, Control and Surveillance System of the Mangrove Clear-Cutting on the Ecuadorian Continental Coast sponsored by the National Chamber of Aquaculture (Camara Nacional de Acuacultura). Both projects were administered by Fundación Natura Capítulo. We are greatful to the Ecuasal Company, for giving permission to do the census and field work within their property. The census work and the banding project were carried out with financial help from the US Fish and Wildlife Service, the Canadian Wildlife service and the Manomet Centre for conservation Sciences. Special thanks to Brian Harrington, Robert Elner

and Ron Ydenberg for stimulating our conservation efforts in Ecuador.

Black-bellied Whistling-Duck *Dendrocygna autumnalis*  Fulvous Whistling-Duck *Dendrocygna bicolor*  Comb Duck *Sarkidiornis melanotos* 

Torrent Duck *Merganetta armata*  Blue-winged Teal *Anas discors* 

White-cheeked Pintail *Anas bahamensis*  Yellow-billed Pintail *Anas georgica*  Andean Teal *Anas andium* 

Masked Duck *Nomonyx dominicus*  Ruddy Duck *Oxyura jamaicensis* 

Least Grebe *Tachybaptus dominicus* 

Horned Screamer *Anhima cornuta* **Least Concern** 

Orinoco Goose *Neochen jubata* **Near-threatened**  Muscovy Duck *Cairina moschata* **Near-threatened**

Cinnamon Teal *Anas cyanoptera* Extirpated Northern Shoveler *Anas clypeata* Rare/Accidental

Southern Pochard *Netta erythrophthalma* **Least Concern**  Lesser Scaup *Aythya affinis* Rare/Accidental

Order: Family/common name Species Remarks/**Global** 

**conservation status**

problem within the GMR.

**7. Acknowledgements** 

ANSERIFORMES: Anhimidae

ANSERIFORMES: Anatidae

PODICIPEDIFORMES:

Podicipedidae


**conservation status**

Order: Family/common name Species Remarks/**Global** 

Snowy Egret *Egretta thula* Common Little Blue Heron *Egretta caerulea* Locally common Tricolored Heron *Egretta tricolor* Common Cattle Egret *Bubulcus ibis* Common

Striated Heron *Butorides striata* Locally Common

Whistling Heron *Syrigma sibilatrix* Rare/Accidental

White Ibis *Eudocimus albus* Locally Common Scarlet Ibis *Eudocimus ruber* Rare/Accidental

Bare-faced Ibis *Phimosus infuscatus* Rare/Accidental Black-faced Ibis *Theristicus melanopis* **Least Concern**  Roseate Spoonbill *Platalea ajaja* Very locally common

Galapagos Rail *Laterallus spilonotus* Endemic/**Vulnerable** Clapper Rail *Rallus longirostris* **Least Concern** 

Brown Wood-Rail *Aramides wolfi* **Vulnerable**  Rufous-necked Wood-Rail *Aramides axillaris* **Least Concern** 

Colombian Crake *Neocrex colombiana* **Data deficient** 

Black-crowned Night-Heron *Nycticorax nycticorax* Common Yellow-crowned Night-Heron *Nyctanassa violacea* Common

Little Egret *Egretta garzetta* 

Green Heron *Butorides virescens* 

Capped Heron *Pilherodius pileatus* 

Boat-billed Heron *Cochlearius cochlearius* 

Glossy Ibis *Plegadis falcinellus* 

Green Ibis *Mesembrinibis cayennensis* 

Rufous-sided Crake *Laterallus melanophaius*  White-throated Crake *Laterallus albigularis*  Gray-breasted Crake *Laterallus exilis* 

Virginia Rail *Rallus limicola* 

Gray-necked Wood-Rail *Aramides cajanea*  Red-winged Wood-Rail *Aramides calopterus*  Uniform Crake *Amaurolimnas concolor*  Chestnut-headed Crake *Anurolimnas castaneiceps*  Russet-crowned Crake *Anurolimnas viridis*  Black-banded Crake *Anurolimnas fasciatus*  Sora *Porzana carolina* 

Paint-billed Crake *Neocrex erythrops*  Spotted Rail *Pardirallus maculatus*  Blackish Rail *Pardirallus nigricans* 

Agami Heron *Agamia agami* 

PELECANIFORMES: Threskiornithidae

GRUIFORMES: Rallidae


**conservation status**

Rare/Accidental/**Data** 

**deficient**

Order: Family/common name Species Remarks/**Global** 

Band-rumped Storm-Petrel *Oceanodroma castro* Accidental Wedge-rumped Storm-Petrel *Oceanodroma tethys* Common Black Storm-Petrel *Oceanodroma melania* Common

Least Storm-Petrel *Oceanodroma microsoma* Accidental

Red-billed Tropicbird *Phaethon aethereus* Coastal Accidental

Jabiru *Jabiru mycteria* Rare/Accidental

Magnificent Frigatebird *Fregata magnificens* Common Great Frigatebird *Fregata minor* Coastal rare

Nazca Booby *Sula granti* Common Blue-footed Booby *Sula nebouxii* Common Peruvian Booby *Sula variegata* Common Red-footed Booby *Sula sula* Coastal Rare Brown Booby *Sula leucogaster* Hypothetical

Neotropic Cormorant *Phalacrocorax brasilianus* Common

Brown Pelican *Pelecanus occidentalis* Common

Pinnated Bittern *Botaurus pinnatus* **Least Concern** 

Cocoi Heron *Ardea cocoi* Coastal common

Great Egret *Ardea alba* Common

Flightless Cormorant *Phalacrocorax harrisi* Endemic/**Endangered**

Guanay Cormorant *Phalacrocoraxbougainvillii* Rare/**Near-threatened**

Peruvian Pelican *Pelecanus thagus* Common/**Near-threatened**

Markham's Storm-Petrel *Oceanodroma markhami* 

Wood Stork *Mycteria americana* 

Anhinga *Anhinga anhinga* 

Zigzag Heron *Zebrilus undulatus*  Least Bittern *Ixobrychus exilis*  Rufescent Tiger-Heron *Tigrisoma lineatum*  Fasciated Tiger-Heron *Tigrisoma fasciatum*  Great Blue Heron *Ardea herodias* 

PHAETHONTIFORMES:

CICONIIFORMES: Ciconiidae

SULIFORMES: Fregatidae

SULIFORMES: Sulidae

SULIFORMES: Anhingidae

PELECANIFORMES: Ardeidae

PELECANIFORMES:

Pelecanidae

SULIFORMES: Phalacrocoracidae

Phaethontidae

Ashy Storm-Petrel *Oceanodroma homochroa* Rare/Accidental **Endangered**


**conservation status**

Order: Family/common name Species Remarks/**Global** 

Wattled Jacana *Jacana jacana* Locally Common

Wandering Tattler *Tringa incana* Locally Common

Upland Sandpiper *Bartramia longicauda* Coastal accidental

Surfbird *Aphriza virgata* Locally common Red Knot *Calidris canutus* Accidental Sanderling *Calidris alba* Common Semipalmated Sandpiper *Calidris pusilla* Common

Western Sandpiper *Calidris mauri* Locally Common

White-rumped Sandpiper *Calidris fuscicollis* Coastal accidental

Imperial Snipe *Gallinago imperialis* **Near-threatened**  Wilson's Phalarope *Phalaropus tricolor* Locally Common

Least Seedsnipe *Thinocorus rumicivorus* Rare/Accidental

Red-necked Phalarope *Phalaropus lobatus* Common Red Phalarope *Phalaropus fulicarius* Accidental

Spotted Sandpiper *Actitis macularius* Common

Greater Yellowlegs *Tringa melanoleuca* Common Willet *Tringa semipalmata* Common Lesser Yellowlegs *Tringa flavipes* Common

Whimbrel *Numenius phaeopus* Common Hudsonian Godwit *Limosa haemastica* Accidental Marbled Godwit *Limosa fedoa* Rare/Accidental

Ruddy Turnstone *Arenaria interpres* Common Black Turnstone *Arenaria melanocephala* Rare/

Least Sandpiper *Calidris minutilla* Common

Baird's Sandpiper *Calidris bairdii* Accidental Pectoral Sandpiper *Calidris melanotos* Accidental Curlew Sandpiper *Calidris ferruginea* Rare/Accidental Stilt Sandpiper *Calidris himantopus* Locally Common Buff-breasted Sandpiper *Tryngites subruficollis* **Near-threatened**  Short-billed Dowitcher *Limnodromus griseus* Locally Common

Long-billed Dowitcher *Limnodromus scolopaceus* Rare

South American Snipe *Gallinago paraguaiae*  Noble Snipe *Gallinago nobilis*  Andean Snipe *Gallinago jamesoni* 

Rufous-bellied Seedsnipe *Attagis gayi* 

CHARADRIIFORMES:

Thinocoridae

Solitary Sandpiper *Tringa solitaria* 

CHARADRIIFORMES:

CHARADRIIFORMES:

Jacanidae

Scolopacidae


**conservation status**

Rare/Accidental/**Near-**

**threatened**

Order: Family/common name Species Remarks/**Global** 

Purple Gallinule *Porphyrio martinica* Locally Common

Common Moorhen *Gallinula chloropus* Locally Common American Coot *Fulica americana* **Extirpated** 

Slate-colored Coot *Fulica ardesiaca* Coastal Accidental

Peruvian Thick-knee *Burhinus superciliaris* Locally common

Collared Plover *Charadrius collaris* Locally common Snowy Plover *Charadrius alexandrinus* Locally Common Wilson's Plover *Charadrius wilsonia* Locally Common

Killdeer *Charadrius vociferus* Locally Common Tawny-throated Dotterel *Oreopholus ruficollis* Extirpated

American Oystercatcher *Haematopus palliatus* Locally Common

Black-necked Stilt *Himantopus mexicanus* Common American Avocet *Recurvirostra americana* Rare

Semipalmated Plover *Charadrius semipalmatus* Common

Andean Lapwing *Vanellus resplendens* Rare Black-bellied Plover *Pluvialis squatarola* Common American Golden-Plover *Pluvialis dominica* Accidental Pacific Golden-Plover *Pluvialis fulva* Rare

Plumbeous Rail *Pardirallus sanguinolentus* 

Azure Gallinule *Porphyrio flavirostris* 

Sungrebe *Heliornis fulica* 

Sunbittern *Eurypyga helias* 

Limpkin *Aramus guarauna* 

Gray-winged Trumpeter *Psophia crepitans* 

Pied Lapwing *Vanellus cayanus*  Southern Lapwing *Vanellus chilensis* 

Piping Plover *Charadrius melodus* 

GRUIFORMES: Heliornithidae

EURYPYGIFORMES:

GRUIFORMES: Aramidae

GRUIFORMES: Psophiidae

CHARADRIIFORMES:

CHARADRIIFORMES:

CHARADRIIFORMES: Haematopodidae

CHARADRIIFORMES: Recurvirostridae

Eurypygidae

Burhinidae

Charadriidae


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Alava, J.J.; Arosemena, X. & Angel, R. (2007). Brown Wood-rail *Aramides wolfi* at El Canclon

Alava, J.J.; Arosemena, X.; Astudillo, E.; Costantino, M.; Peñafiel, M. & Bohorquez, C. (2007).

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*canclón, Anhima cornuta y su habita en la Reserva Ecológica Manglares Churute, Ecuador*. PPD-PNUMA, Fundación Natura Capitulo Guayaquil, REMCH, Ministerio del

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Lagoon, Manglares-Churute Ecological Reserve, Ecuador. *Cotinga*, Vol. 27, pp. 81-

Occurrence, abundance, and notes on some threatened Ecuadorian birds observed in the El Canclon Lagoon, Manglares Churute Ecological Reserve. *Ornitologia* 

seasonality and conservation threats of the Horned Screamer (*Anhima cornuta*) in Southwestern Ecuador. *Waterbirds* Vol.32, No. 1, (March 2009), pp.81-86, ISNN

(2010). Observations, distribution and potential threats to the Mangrove Black Hawk *Buteogallus anthracinus subtilis* in mangrove habitat of southwestern Ecuador. *Boletín de la Sociedad Antioqueña de Ornitología (Boletin SAO)* Vol. 20, No.2, *In press*,

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*British Columbia, Canada*. PhD Thesis, School of Resource and Environmental Management, Faculty of Environment, Simon Fraser University, BC, Canada.

**8. References** 

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671*,* ISSN 0025-326X


Annex I. List of waterbird species of Ecuador, including species of the Galapagos Islands Scientific and English names follow the South American Classification Committee (SACC) Classification, Version 31 March 2011 (Freile, 2010).
