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Revista Brasileira de Ornitologia, 24(2), 94-115 article June 2016

Breeding populations in Brazilian oceanic : historical review, update and a call for census standardization

Patrícia L. Mancini1,3, Patrícia P. Serafini2 and Leandro Bugoni1

1 Laboratório de Aves Aquáticas e Tartarugas Marinhas, Instituto de Ciências Biológicas, Universidade Federal de Rio Grande - FURG, CP 474, CEP 96203-900, Rio Grande, RS, Brasil. 2 Centro Nacional de Pesquisa e Conservação de Aves Silvestres - CEMAVE/ICMBio/MMA. Base Multifuncional CEMAVE/SC. Rodovia Maurício Sirotsky Sobrinho s/nº, km 02, SC 402, trevo Jurerê, CEP 88053-700, Florianópolis, SC, Brasil. 3 Corresponding author/Current address: Seção de Aves, Museu de Zoologia da Universidade de São Paulo, Av. Nazaré, 481, Ipiranga, CEP 04263- 000, São Paulo, SP, Brasil. email: [email protected]

Received on 12 October 2015. Accepted on 21 April 2016.

ABSTRACT: In recent decades, several seabird populations have declined globally due to anthropogenic activities. In , 14 seabird breed at four oceanic islands and one atoll: the Abrolhos, Fernando de Noronha, and São Pedro and São Paulo (SPSPA) archipelagos; the Trindade/Martin Vaz Islands; and the Atol das Rocas. Seven species are listed as nationally threatened by extinction. This study aimed to present new information on breeding seabird populations in Brazilian oceanic islands, compile all available data previously published and, when possible, to provide updated information on population estimates from censuses carried out sporadically at different islands between 2006 and 2013. Based on new data and the thorough review provided here, of the 35 seabird breeding populations analysed, 14% were increasing (as Red-billed Phaethon aethereus, Magnificent Fregata magnificensand Anous stolidus in Abrolhos), 11% were decreasing (as Brown Sula leucogaster in Atol das Rocas and Fregata minor in Trindade ), 23% were stable (as White-tailed Tropicbird Phaethon lepturus in Fernando de Noronha and Brown Noddy and Anous minutus in São Pedro and São Paulo Archipelago), and the remaining 49% were unknown or not possible to evaluate. The Red-footed Booby (Sula sula) is locally extinct in Trindade Island, however there are colonies of only a few individuals of other species, such as the Audubon's Shearwater Puffinus lherminieri and Red- billed Tropicbird in Noronha, Black Noddy in Martin Vaz, and Great (Fregata ariel trinitatis) and Lesser (F. m. nicolli) in Trindade, that may become extinct soon. Censuses at distinct periods of the breeding cycles and protocols were highly variable, making temporal comparisons difficult. These results indicate an urgent need for long-term studies to improve the scenario to assess seabird population trends based on comparable methodologies, in to determine trends in the future.

KEY-WORDS: booby, frigatebird, noddy, petrel, tern.

INTRODUCTION there is an urgent need for data on population sizes and distribution to assess trends over time to properly infer Of the 346 seabird species in the world, 114 (33%) the for species and populations not are globally threatened and 10% are listed as “near yet assessed. However, trends are hard to measure without threatened” (Croxall et al. 2012). In addition, about prior data (Bibby et al. 1998), so regular standardized 70% of world seabird populations declined among the censuses are fundamental tools to investigate seabird 19% of seabird populations monitored regularly between population trends. 1950 and 2010 (Paleczny et al. 2015). Globally there Several approaches to estimate the abundance of are 1352 threatened breeding seabird populations of 98 have been used, including at-sea counts (Woehler species, from 986 islands (Spatz et al. 2014). The main 1996) and counts on wintering roosting sites (Bugoni threats for seabirds are commercial fisheries (bycatch and & Vooren 2005). However, counting nests at breeding competition for prey), habitat degradation, introduction sites is assumed to be the most reliable way to monitor of alien species to their breeding grounds, pollution, and population trends of seabirds over time (Hutchinson climate change (Croxall 2008, Grémillet & Boulinier 1979, Bibby et al. 1998), although it is not always possible 2009, Croxall et al. 2012, Lewison et al. 2012, Quillfeldt due to nest inaccessibility for some species, disturbance & Masello 2013, Wilcox et al. 2015). Consequently, causing nest failure, lack of funds, or because it is time-

Revista Brasileira de Ornitologia, 24(2), 2016 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization 95 Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

consuming or inaccurate (Hutchinson 1979). Thus, other Itatiaia archipelago (in Espírito Santo state, in August methodologies to estimate population sizes can be used 1993), but there is no further record since then (Efe & when counting nests is not possible, but it is essential that Musso 2001). The Red-footed Booby breeds only in standardization be considered to compare population Fernando de Noronha (Antas 1991, Schulz-Neto 2004), numbers (Vooren & Chiaradia 1990, van Franeker 1994, as now it seems extirpated from Trindade Island (Fonseca- Yorio et al. 1994, Bibby et al. 1998). Neto 2004, this study). The Red-billed Tropicbird breeds About 38% of the seabird species recognized mainly in Abrolhos with a few individuals breeding in globally occurs in Brazil as breeders, migrants or vagrants Fernando de Noronha, while the White-tailed Tropicbird (Piacentini et al. 2015). Seabird colonies are generally breeds mainly in Fernando de Noronha, with a few located on islands, cliffs or headlands (Schreiber & Burger individuals breeding in Abrolhos (Oren 1984, Antas 2002, Nelson 2005). In Brazil, 14 seabird species breed at 1991, Sick 1997). Furthermore, Trindade Island is the the four offshore islands and one atoll (from now on called only known nesting area of ​​the subspecies Fregata ariel oceanic islands): Fernando de Noronha, and São Pedro trinitatis and Fregata minor nicolli (Orta et al. 2014a,b,c). and São Paulo (SPSPA) archipelagos; Trindade Island Despite a 25-year-old study on the status of Brazilian together with Martin Vaz, the Abrolhos Archipelago over seabirds (Antas 1991), estimates of seabird populations the continental shelf and Atol das Rocas (Antas 1991, in Brazilian offshore islands have never been determined. Vooren & Brusque 1999). The most important breeding Antas (1991) provided the first whole national assessment areas in terms of the number of species and abundance of seabird populations, based on his experience and the are the Fernando de Noronha Archipelago and Atol das scarce available data at that time. The limited data from Rocas (Antas 1991, Schulz-Neto 2004). Eleven species random counting were used for the assessments, which breed in Fernando de Noronha, eight in Abrolhos, eight lacked of standardized methods. Some counts for specific in Trindade and the Martin Vaz Islands, five in Atol das islands, colonies and species were available before or Rocas, and three in SPSPA (Antas 1991, Schulz-Neto after this time, but lacking in regularity and standardized 1998, 2004, Both & Freitas 2004). Despite such variety, methodology (e.g. Fernando de Noronha - Oren 1984, there is only one globally threatened seabird species Antas 1991, Schulz-Neto 2004; Atol das Rocas - Antas breeding in Brazil, the Trindade Petrel (Pterodroma 1991, Schulz-Neto 1998; Abrolhos - Antas 1991, Alves et arminjoniana), listed as “Vulnerable” by the IUCN al. 2004, Fonseca-Neto 2004; and Trindade/Martin Vaz (2014) and nationally as “” by Islands - Olson 1981, Fonseca-Neto 2004, Luigi et al. Ministério do Meio Ambiente (MMA 2014). However, 2009). The only exception is SPSPA (Mackinnon 1962, 7 out of 14 species breeding in Brazilian offshore islands Masch 1966, Smith et al. 1974, Edwards et al. 1981, are considered nationally threatened and three of them Antas 1991, Both & Freitas 2004, Barbosa-Filho & are “Critically Endangered” according to the recent Vooren 2010), mainly for the population, Brazilian Red List (MMA 2014). for which whole island counts have been carried out Most species breeding in Brazilian offshore islands regularly since early 2000s. are widely distributed in tropical and subtropical oceans, This study aims to evaluate population data for such as the Brown Noddy (Anous stolidus), Black Noddy 14 seabird species breeding in Brazilian oceanic islands, (Anous minutus), (Onychoprion fuscatus), based on a thorough literature review and counts carried White Tern (Gygis alba), Brown Booby (Sula leucogaster), out during 14 irregular expeditions, from 2006 to 2013, (Sula dactylatra), Red-footed Booby to assess if these studies used methods that could provide (Sula sula), White-tailed Tropicbird (Phaethon lepturus), a national picture of population sizes and trends. The Red-billed Tropicbird (Phaethon aethereus), Magnificent initial motivation for a detailed compilation had been Frigatebird (Fregata magnificens), Great Frigatebird the need to reassess conservation status of species at the (Fregata minor), and (Fregata ariel) (del national level for the Brazilian Red List (MMA 2014). Hoyo et al. 1992). However, comparatively, some species Additionally, we suggest standardized methodologies for have smaller global distributions such as the Trindade long-term monitoring of such populations, to improve Petrel and Audubon's Shearwater (Puffinus lherminieri). the scenario of their trends in the future and thus better The Trindade Petrel breeds on Trindade Island offshore subsidize conservation actions. in Brazil (Espírito Santo state), and which during the last century colonized Round Island in the (Brown et al. 2010, 2011). Audubon's Shearwater is METHODS distributed in tropical and subtropical areas of the West Atlantic Ocean (Carboneras et al. 2014), but in Brazil Seabird censuses were carried out in sporadic visits to the breeds regularly only in Fernando de Noronha archipelago islands between 2006 and 2013, during 14 expeditions, (Antas 1991). This species was reported breeding at including four in Fernando de Noronha (two in

Revista Brasileira de Ornitologia, 24(2), 2016 Revista Brasileira de Ornitologia, 24(2), 2016 96 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

partnership with CEMAVE - Centro Nacional de Pesquisa censuses on-board a motorboat were performed in August e Conservação de Aves Silvestres), four in SPSPA, two in (6 h observation), November 2010 (4 h), and April 2011 Abrolhos, two in Atol das Rocas, and two in Trindade (4 h) with 10 × 50 mm binoculars to count seabirds flying Island (Figure 1, Tables 1 & 2). The censuses were or roosting on the northeast coast of the main island and conducted between 05:30 h and 08:30 h and between islets. Furthermore, for some species, such as 16:30 h and 18:30 h, when the majority of seabirds were and petrels, nests were actively searched in Fernando de in the colony (Schulz-Neto 2004). For breeding species, a Noronha, Abrolhos, and Trindade. For those species with stick was used to disturb adults and verify the presence of a limited number of individuals and nesting in inaccessible or chicks. In almost all colonies (Table 2), censuses places, such as both frigatebird species from Trindade, the were performed by direct counting of individuals and nests maximum counts of flying individuals and individual (Bibby et al. 1998). This study used the direct counting characteristics (male/female, juveniles/adults) of nests, but in order to compare with prior data, it was were used for a rough estimate of the minimum number necessary to convert nests to number of individuals (1 nest of individuals. = 2 individuals). In colonies with high seabird densities An extensive literature review was performed to (e.g. Sooty Tern in Atol das Rocas), were counted gather data of breeding seabird population abundance in random quadrats (100 m2) with different densities, (individuals or nests) in Brazilian oceanic islands. and the mean number of individuals was calculated and Published articles, thesis, and conference abstracts in subsequently extrapolated for the total area occupied by English and Portuguese from 1936 to 2014 were used the colony (Bibby et al. 1998). In Fernando de Noronha, (Appendix I).

FIGURE 1. Location of the Brazilian offshore islands where the seabird population censuses were performed and the breeding seabird richness for each island/archipelago.

Revista Brasileira de Ornitologia, 24(2), 2016 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization 97 Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

TABLE 1. Period of seabird censuses during expeditions carried out in each Brazilian offshore archipelago or island. - no census.

Island Expedition I Expedition II Expedition III Expedition IV

Abrolhos 20 February–06 March 7–20 August - - 2011 2011

Atol das Rocas 05 September–04 October 13 February–06 March - - 2010 2012

Fernando de Noronha 04–10 August 23–28 November 20 March–11 April 08 July–02 August 2010 2010 2011 2011

São Pedro and São Paulo 14–27 August 9–22 August 2011 06–17 January 1–30 June (SPSPA) 2010 2012 2013

Trindade Island 28–29 June 16 December 2006–25 - - 2006 April 2007

TABLE 2. Seabird species recorded in their respective breeding sites in Brazilian offshore islands. X = presence, “-” = absence, E = extinct, SPSPA = São Pedro and São Paulo.

Fernando de Atol das Trindade and No. of Breeding species SPSPA Abrolhos Noronha Rocas Martin Vaz Islands islands

Pterodroma arminjoniana1 - - - - X 1 Puffinus lherminieri2 - X - - - 1 Phaethon aethereus3 - X - X - 2 Phaethon lepturus3 - X - X - 2 Sula dactylatra - X X X X 4 Sula leucogaster X X X X - 4 Sula sula3 - X - - E 1(1) Fregata magnificens - X - X - 2 Fregata ariel trinitatis2 - - - - X 1 Fregata minor nicolli2 - - - - X 1 Anous minutus X X X - X 4 Anous stolidus X X X X X 5 Gygis alba - X - - X 2 Onychoprion fuscatus - X X X X 4 Total spp. per island 3 11 5 7 8(1) 1 Listed as globally “Endangered” (IUCN 2014) and nationally “Critically Endangered” (MMA 2014); 2 Listed as nationally “Critically Endangered” (MMA 2014); 3 Listed as nationally “Endangered” (MMA 2014).

Results are presented as the number of individuals Results of new censuses are presented together with data per species and archipelago. In order to make all censuses from previous studies, but a statistical evaluation of trends comparable, when the nest was the basis for counting, over time was not attempted, as census procedures differed we considered each to indicate two individuals, in line markedly among studies, and frequently lack detailed with the predominantly monogamous breeding system of information on protocols, census effort, seasonality and seabirds (Schreiber & Burger 2002). In the case of the covered area. Reliable estimates for the current overview direct counting of nests or individuals in the same area are those of Brown at SPSPA, a small place with for the same species in the same expedition, we used the a full-time presence of researchers at a scientific station. higher count as the estimated maximum number for the Other good estimates were those of both tropicbird expedition. In Fernando de Noronha, for most seabird species in Fernando de Noronha and Abrolhos. Estimates populations, censuses were possible only in some areas, for these species were based on nest counts (through nest which underestimated the actual seabird population sizes. mapping), a laborious task undertaken with support

Revista Brasileira de Ornitologia, 24(2), 2016 Revista Brasileira de Ornitologia, 24(2), 2016 98 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

from experienced cliff climbers, an intensive ringing Finally, based on the literature review and our scheme, and a year round research effort. In addition, experience in the field, at the five Brazilian oceanic islands, estimates for these species benefited from their small we summarized most suitable methods and breeding populations. For SPSPA and Abrolhos, whole island nest/ periods as a starting point for national standardization of individual counts were adequate for a reliable and low seabird census on those islands. disturbance estimation of population sizes. At the flat Atol das Rocas, due to the large number of nests, whole ground counts were unrealistic, and the delimitation of RESULTS quadrats for counts and density estimation, followed by extrapolations, were a better option, except for species All seabird population abundance for each species and with limited numbers. More problematic were Fernando islands are in Appendix I. Population trends are in Table de Noronha and Trindade/Martin Vaz due to the size of 3 and further comments as follows. these islands, their rough and steep terrain, and limited access, in addition to several surrounding islets. For these Trindade Petrel Pterodroma arminjoniana places, a species-by-species analysis should be undertaken The Trindade Petrel breeds only at Trindade Island in the before a standard protocol is established. Atlantic Ocean and Round Island in the Indian Ocean In the present study, for population trend (Brown et al. 2011). In Trindade, estimates ranged estimations, only censuses using the same methodology from 2000 individuals in August 1988 (Nacinovic et al. (e.g. direct counts) for a species and site were evaluated. 1989) to 3000–5000 individuals in January–April 2006 The criteria to classify population trends were: Increasing (Luigi et al. 2009), but the lack of detailed information – when data showed an increasing number of individuals from previous censuses precludes trend estimation. The based in censuses carried out in similar periods (e.g. species did not breed on Martin Vaz as suggested in early November 2001 and October 2010) and similar areas; studies. Decreasing – when data showed a decreasing number of individuals based in census carried out in similar periods Audubon's Shearwater Puffinus lherminieri and similar areas; Stable – when data showed little In Fernando do Noronha, a maximum of 30 Audubon's variation (100–200 individuals) based in census carried Shearwaters were counted in October 2005 (Silva-e-Silva out in similar periods and similar areas; Not Determined & Olmos 2010). The population trend for this species (ND) – when census were carried out using different was not determined because nests at Morro do Leão methodology, periods, areas or lacking information, and Island, where about half of reported nests are placed, Extinct (E) – when the species have been not recorded in have not been checked since 2006 due to weather and the past 15 years in their breeding grounds. oceanographic conditions precluding landing.

TABLE 3. Summary of seabird population trends in their respective breeding sites in Brazilian offshore islands. ND = not determined, E = extinct, SPSPA = São Pedro and São Paulo Archipelago. Fernando de Trindade and Breeding species SPSPA Atol das Rocas Abrolhos Noronha Martin Vaz Islands Pterodroma arminjoniana - - - - ND Puffinus lherminieri - ND - - - Phaethon aethereus - ND - Increasing - Phaethon lepturus - Stable - ND - Sula dactylatra - ND ND Stable ND Sula leucogaster Increasing ND Decreasing ND - Sula sula - Stable Increasing* - E Fregata magnificens - ND Stable* Increasing - Fregata ariel trinitatis - - - - ND Fregata minor nicolli - - - - Decreasing Anous minutus Stable ND Decreasing - ND Anous stolidus Stable ND Decreasing Increasing Stable Gygis alba - Stable - - ND Onychoprion fuscatus - ND ND Stable Increasing * Non-breeding population; - Non-breeding in this island.

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Breeding seabird populations in Brazilian oceanic islands: historicald review,500 update and440 a call for census standardization 99 n

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Patrícia L. Mancini, Patrícia P. Serafinif and Leandro Bugoni

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population increased in the whole area (Figure 2). d i 8000 Atol das Rocas v 1850 i 1500 800 Abrolhos 4 d n 1591 i 7000 1600 6400

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White-tailed Tropicbird Phaethon lepturus N 100 100 200 140 105 The population in Fernando de Noronha in December 100 170 175 1982 0was estimated at 200 individuals (Oren 1984), 70 Apr.1981 Jun.1992 Feb.2011 Aug.2011 2011 0 Fernando de Noronha 0 which400 was similar to census results from August 2010 and 8 9 0 2 3 8 1 0 1 1 (bimonthly) 8 9 0 0 0 0 0 1 1 1 9 9 0 0 0 0 2 0 0 0 s 1 1 2 2 .2 .2 . .2 .2 .2 l . . . . c t g n r b g v r l a 300 c a u a u August 2011 to January 2012 (Figure 3). Censuses from e O u Ju Fe A o J u D A M N M

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m b 100 62 u 18 22 Jul.1994 Feb.2011 Aug.2011 N 53 0 FIGURE 4. Population trends of the Masked Booby Sula dactylatra in Atol das Rocas from April 1991 (Schulz-Neto 1998) to February/ March 2012; in Fernando de Noronha archipelago, from December 19888 0(Antas0 1991)Ferna ntod oJuly de N2011oron andha in Abrolhos archipelago from July 1994700 (Alves et al. 2000) to August 2011, through direct counting.

FIGURE 3. Population trend of the White-tailed Tropicbird Phaethon s l

S-Oa = September to October; F-M = February to March.

lepturus in Fernando de Noronha from December 1982 (Oren 1984) u 600 550 600 d i v

August 2011 to January 2012 (present study, M. A. Efe unpublished i

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Revista Brasileira de Ornitologia, 24(2), 2016 Revista Brasileira de Ornitologia, 24(2), 2016 8000 Atol das Rocas 7000 6400 s l a

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N 2000 1248 1000 1600 1600 0 Apr.1991 Nov.1991 Sep.1994 2000-2002 S-O.2010 F-M.2012 100 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

5 differences400 Ainto lthe da s periodRocas of the year among censuses data. Red-footed Booby Sula sula s l 350 5 Browna 400 BoobyAto l breedsdas Roc ains other300 coastal islands along the In Fernando de Noronha, the population trend was stable, u 300 d i

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m b 200 r d u

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i 3000 N 100 resting. In Atol das Rocas, a maximum of 350 birds were 1 2 f 2 0 9 1 4 1 1205 1 2580 m b 8 9 9 9 9 0 1 0 o 9 9 9 9 0 0 u 76 0 .1 .1 .1 .1 .1 2 .2 .2 r 1658

N v r e 100 b b o p p ct M recorded2000 in September 2010, showing an increasing trend e 2 e 0 1 1 e 4 1 1205 - 2 1440 F 8 F 9 N 9 A 9 S 9 0 O 1 F 1 1184

9 9 76 9 9 9 0 0 0 m b 0 1 1 1 1 1 2 2 2 1882 ...... (Figureu 6), while in SPSPA roosting birds varied from 7one33 b b v 1 r p t M 2 1000 1513 1511 2 0 o p 1 4 1 c 0 N e 8 e 9 9 9 e 9 0 1 - 1 F 9 F 9 N 9 A 9 S 9 0 O 0 F 0 0 .1 .1 .1 .1 .1 2 .2 .2 to nine individuals from 2000 to 2013. Also, the Red- b b v r p t M e 2 e 0 o 1 p 1 e 4 1 c 0 - 2 F 8 F 9 N 9 A 9 S 9 0 O 1 6F 1 0 700 9 SPSPA9 9 9 9 0 0 0 footed Booby used to breed on Trindade Island, but birds .1 .1 .1 1 .1 2 2 .2 b b v r. p t. e e o p e c -M

s F F N A S O F 588 were not seen since 2000 (Fonseca-Neto 2004) and from l 7600 SPSPA a u

d December 2006 to April 2007 (this study) or thereafter, i s SPS5P0A0 500 588 l v 65700 546 i a d u 439 420 so the species is assumed to be extinct in the island. n d i s 588 i

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0 100 100 600 Abrolhos 50 600 Abrolhos 0 s l 500 460 Feb.1982 Apr.1991 Nov.1991 Sep.1994 Sep.2010 F-M.2012 a

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i 300 u e r 1658 f e N 400 186 2000 1440

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r 100 230 1184 m b u 300 1882 e u N 200 186 1000 1513 1511 733 N

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N 0 200 186 0 100 1293609 Jul.1994 Feb.2011 Aug6.2011 0 186 100 1969 Jul.1994 Feb.2011 Aug.2011 0 1969 Jul.1994 Feb.2011 Aug.2011 10000 Fernando de Noronha s l 1969 Jul.1994 Feb.2011 Aug.2011

a 870 1000 Fernando de Noronha FIGURE 6. Population trends of the Red-footed Booby Sula sula u 800 d i

s 400 Atol das Rocas l v in Atol das Rocas from December 1982 (Antas 1991) February i a 1000 F8e7r0nando de Noronha 350 d s u 800 l n d a

i and March 2012 and in Fernando de Noronha Archipelago from s 600 i

l u f v

a 870 i d o 1000 Fernando de Noronha u i

d 800 December 1982 (Oren 1984) to July 2011, through direct counting. r v d n i i s e i 600

l 300

v 400 d 253 f i a 870 F-M = February to March. 269 n o d i u m b

800 n r f d u i

i 600

e o v f

N 400 i 200 r 201 o d

269 80 98 e

m b 81 66 61 r n

i 600 u e 400 8 200 f Fregata magnificens m b N

o 200 269 u

m b 0 80 98 200 r 81 66 61 N u e 400 0 1 2 3 0 0 1 8 In Fernando de Noronha, recent censuses did not cover N 9 0 1 1 1 200 9 9 0 0 1 0 0 1 9 1 080 2269 908 2 2 0 m b 1 . 81 2 . 2 .66 . 61 0 . v . r g. v r .2 u b o n a o a l Sela Gineta Island (the only breeding colony) due to e 1 u 3 u 0 0 1 Ju 8 100 100 N F 0 N 9 J 2 M 0 A N 1 M 1 1 200 9 9 0 0 1 0 0 1 0 9 1 080 2 908 2 2 0 .1 . 81 .2 r. .2 .66 r. 61 2 weather and oceanographic conditions, precluding trend FIGURE b5. v a g v a 1 l. e Population0 o 1 trendsn 2 of the3 Brownu 0 Boobyo 0 Sula leucogasteru 8 1 in F 9 N 9 Ju 0 M 0 A 1 N 1 M 1 J 1 9 9 0 0 0 0 0 0 50 0 1 .1 2 .2 .2 .2 .2 2 estimation (Figure 7). In Atol das Rocas, the species also Atol das Rocas. fromv February. 1982r (Antasg 1991)v to F-Mr = Februaryl. to b o 1 n a 3 u o 0 a 1 e 0 N 9 Ju 2 M 0 A 0 N 1 M 1 Ju 1 0 F 9 9 0 0 1 0 0 1 March 2012;9 in São1 Pedro and0 São2 Paulo Archipelago0 2 from2 November0 forages and rest, but does not breed, and the maximum .1 . .2 r. .2 . r. 2 Feb.1982 Apr.1991 Nov.1991 Sep.1994 Sep.2010 F-M.2012 b v n a g v a l. 1960 (Mackinnone o 1962)u to June 2013; uin Abrolhoso Archipelagou from F N J M A N M J number of individuals reported was 50 in February 1982 1969 (Coelho 1981) to August 2011; and in Fernando de Noronha (Antas 1991). In Abrolhos, the population trend was archipelago from February 1990 (Antas 1991) to July 2011, through direct counting. F-M = February to March; S-N = September to increasing based on censuses carried out in March 1994 November; M-J = March to July. and February 2011 (230 and 660 birds, respectively) and

Revista Brasileira de Ornitologia, 24(2), 2016 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization 101 Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

October 1994 and August 2011 (332 and 854 birds, Island; however, in 1975–1976 no colonies were respectively,1000 A Figurebrolhos 7). recorded and only a small group of 15 Lesser Frigatebird Abrolhos 854 1000 nests (Olson 1981). Since then, there have been no 7 1000 Abrolhos 854 s

l 800 7 a 854 further reports of either species nesting on the island, u s l

d 800 i a v

u although there have been several reports of frigatebirds i s

l 800 d d i

a 600

n 660 v u i i observed in flight (Orta et al. 2014b,c), including a record d f d i 600 o n v 660

i i

r f d of 120 individuals attending a vessel for discards near e 600 332 o n 400 660 b

i

r f m

e 332

o Ponta Noroeste in August 1994 (Fonseca-Neto 2004).

u 400

b r N m e 332

u 400 b 200 Only three individuals were recorded from December N m 230 u 200 2006 to April 2007, indicating a severe long-term decline N 120 230 200 0 120 230 (Appendix I). 0 Apr.1918210 Mar.1994 Oct.1994 Feb.2011 Aug.2011 0 Apr.1981 Mar.1994 Oct.1994 Feb.2011 Aug.2011 Black Noddy Anous minutus late 1980 Mar.1994 Oct.1994 Feb.2011 Aug.2011 In SPSPA, the Black Noddy population trend was stable Atol das Rocas 70 (Figure 8). In Fernando de Noronha, the recent censuses s l 70 Atol das Rocas a 60 s 600 SPSPA u l s

l did not cover all the areas where this species occurs in d a

i 50 a u

v 60 u i 50 d i d d the archipelago, precluding further analysis. In Atol das i 50 v 500 n i v i

i 481

50 8 d f d 40 40 n o Rocas,i population trend seem to be decreasing: 1,750 n

i f

r

f 366

o 400 e

40 40 o b r 30 individuals in September 1994 (Schulz-Neto 1998) and r e m

e 20 u b 30

886m b individuals in October 2010 (Figure 8). The species N 20 300 m 15 20 u 320

u 300 N N 20 7 15 does not breed on Trindade Island, but a relict population 10 200 7 12 10 persists on Ilha do Norte150 at Martin Vaz, where about 10 0 12 165 nests1 0were0 photographed on an inaccessible cliff in April 0 Feb.1982 Nov.1991 Apr.1991 Sep.1994 S-O.2010 F-M.2012 Feb.1982 Nov.1991 Apr.1991 Sep.1994 S-O.2010 F-M.2012 2007. Based on nests and individuals flying nearby, a 0 resident populationNov.1960 May of197 about1 Sep.1 92079 individuals1999-2000 J-A .is 20 expected00 Aug.201 to0 600 Fernando de Noronha persist at this place. No previous estimate for the island

s Fernando de Noronha

l 600

a 500 was available. u s l d 430 i a

v 500 u i d d 430 2500 Atol das Rocas i 400 n v i i

s f d 400 300 l o n a

i r

300 u f e

300 d o i 2000

v r

300 i m b e d u

200 n

i 1480 N

m b 122 f

u 200 1750 200 o 1500

1750 N 100 150 r 200 122 e 150 100 m b 0 u 1000 1982 M-J./O-N.1987 Nov.1992 Aug.2010 Nov.2010 N 0 886 1982 M-J./O-N.1987 Nov.1992 Aug.2010 Nov.2010 500 FIGURE 7. Population trends of the Magnificent FrigatebirdFregata magnificensin Abrolhos from late 1980 (Antas 1991) to August 2011; in Atol das Rocas from February 1982 (Schulz-Neto 1998) to March 0 Apr./Nov.1991 Sep.1994 Oct.2010 Feb.-Mar.2012 2012; and in Fernando de Noronha Archipelago from 1982 (Oren 1984) to November 2010, through direct counting. S-O = September

to October; F-M = February to March; M-J = May to June; O-N = s 600 SPSPA l a

October to November. u d i

v 500 i 481

8 d n i

f 366

o 400 Lesser Frigatebird Fregata ariel r The subspecies F. a. trinitatis is restricted to the e m b 300 u 320 300 South Atlantic Ocean and only breeds at Trindade Island. N 200 The last breeding report was in 1975/76, when 15 pairs, 150 165 about 50 individuals, were observed breeding in Trindade 100 Island (Olson 1981). From December 2006 to April 0 2007 a maximum count of two non-breeding individuals Nov.1960 May 1971 Sep.1979 1999-2000 J-A. 2000 Aug.2010 was obtained. FIGURE 8. Population trends of the Black Noddy Anous minutus in Great Frigatebird Fregata minor Atol das Rocas from April to November 1991 (Schulz-Neto 1998) to February–March 2012 and in São Pedro and São Paulo Archipelago 2500 Atol das Rocas The subspecies F. m. nicolli is restricted to the South (SPSPA) from November 1960 (Mackinnon 1962) to August 2010, s l througha direct counting. J-A = July to August. Atlantic Ocean. Great Frigatebirds once bred on Trindade u d

i 2000 v i d n

i 1480

Revista Brasileira de Ornitologia, 24(2), 2016 Revista Brasileira de Ornitologia, 24(2), 2016 f 1750 o 1500

1750 r e m b

u 1000 N 886 500

0 Apr./Nov.1991 Sep.1994 Oct.2010 Feb.-Mar.2012 9 30000 Atol das Rocas 27390 25000

s 18700 l

a 20000 u d

i 17700 v i

d 15000 n i

f o 11800 r

e 10000 10000 b m u 4060 N 5000 3202 400 0 102 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

Brown Noddy Anous stolidus with Fonseca-Neto (2004). Population trends were stable. In SPSPA,600 SthePSP Apopulation trend was stable (Figure 9). The species potentially breeds on Martin Vaz, but the s l

a 500 490

Inu Fernando4 80de Noronha, censuses in this study were island was visited in early April 2007, a period out of the d i v restrictedi 400 to Viuvinha Island and the port39 0 area, which expected breeding season. Breeding at Martin Vaz remains d

n 324 i

precludesf further analysis of the population trends. In Atol to be confirmed. In Trindade Island important breeding

o 300

300 r

dase Rocas, recent censuses indicated a decreasing trend locations include Pão de Açúcar, Pico do Vigia, Ilha do Sul, 200 213 220 m b

(Figureu 9) using the20 0same methodology (random quadrats) Farilhões, Pico do Monumento and the beach southward, inN comparable100 seasons. In Abrolhos, the population Crista do Galo, and the nearby Ponta Norte. increased0 from 2000 individuals in 1982 (Antas 1991) to 0 1 9 0 0 0 0 6 7 9 8 0 0 0 1 9 9 7 9 0 0 0 0 White Tern Gygis alba 4725 in August1 12011 (Figure9 1 9). In 2 Trindade,-2 at.2 least2 250 . y .1 y . 9 r g. v a p a A 9 p u o e J- 9 A nests couldN beM foundS everyM year, based1 on direct counts A or In Fernando de Noronha, the population trend was stable estimated based on adults attending colonies in inaccessible comparing the first census of 250 individuals in December places, which converts to at least 500 individuals, in line 1982 (Oren 1984), with recent counts in November 2010 (252 individuals). In 2011, both censuses covered only 6000 Abrolhos part of the species' distribution in the archipelago and 5000 4725 the population size is underestimated. In Trindade Island

s 3926 nests are scattered on the cliffs and population trends l

a 4000 u 4180

d were estimated due to differences in census seasonality. In i v i

d 3000 Martin Vaz, eggs of at least 15 pairs and about 40 adults n i

f 3000 o

were found in early April 2007. No previous breeding r

e 2000 2000 record was available for this place. m b u

N 1000 Sooty Tern Onychoprion fuscatus 0 In Fernando de Noronha, the population size was 9 30000 ApAr.t1o98l 2das RMoacr.a1s995 1995 1996 Aug.2011 27390 underestimated, precluding trends estimation due to 9 2350000 Atol das Rocas differences in areas and the period of the year when

s 27390 18700 censuses were carried out. In Atol das Rocas, the l

a 20000

u 25000

d population apparently decreased in the latest years (Figure i 17700 v i

s 18700 d l 15000 10). However, an oscillation of an order of magnitude n a

i 20000

u f d o i is suspicious and may reflect methodological issues 17700

v 11800 r i e

d 10000 10000

b 15000 n rather than real trends, thus no trends were estimated. i

m f u o

4060 N 11800 In Abrolhos, population was stable indicating 20 Sooty r 5000 e 10000 10000 b 3202 Terns in early and latest census. The species also breeds m u 400 4060 N 5000 in several colonies on Trindade Island, but the largest 3202 400 concentrations are on the top of Morro do Paredão, 0 Morro das Tartarugas, Praia das Tartarugas, Pico do Monumento, and Parcel. Whole island count and colony size estimation was carried out from December 2006 to 10 April 2007, which resulted in 2924 nests (roughly 6000 600 SPSPA Atol das Rocas

s 160000 l

a 500 490

u 480 s d 600 SPSPA l

i 140000 140000 a v i 400 390 u s d d l 115000 i n

a 490 324

i 500 120000 v

i u 480 f d d

o 300 i 106620

300 n v i r

i 100000

e 400 390 f d o n 324 i 200

213 220 r

m b f e 80000 u

o 300 200 b 300 N 75000 r m

e 100 u 60000 200 213 220 N m b

u 0 200 N 40000 100 0 1 9 0 0 0 0 6 7 9 8 0 0 0 1 9 9 7 9 0 0 0 0 30000 40000 28956 15846 1 1 9 1 2 -2 .2 2 . y .1 y . 9 r g. 20000 v a p a A 9 p u 0 o e J- 9 A N M S M 1 A 0 1 9 0 0 0 0 6 7 9 8 0 0 0 1 0 9 9 7 9 0 0 0 0 1 1 9 1 2 -2 .2 2 9 2 0 1 1 3 0 2 FIGURE 9.. Populationy trends.1 ofy the Brown. Noddy9 Anousr stolidusg. in 7 8 9 9 9 9 1 1 v a p a -A 9 p u 9 9 9 9 9 9 0 0 o e J 9 A .1 1 .1 .1 1 .1 .2 .2 N M S M 1 A r . b r v. b Abrolhos Archipelago from April 1982 (Antas 1991) to August 2011; a eb e p o e ct -M M F F A N F O F in Atol das Rocas from March 1979 (Antas 1991) to February–March 2012;60 0and0 in ASãobro Pedrolhos and São Paulo archipelago (SPSPA) from FIGURE 10. Population trend of the Sooty Tern Onychoprion fuscatus November 1960 (Mackinnon 1962) to August 2010, through direct at Atol das Rocas from March 1979 (Antas 1991) to February–March 5000 4725 counting.6000 J-A A= bJulyrolh toos August. 2012, through random quadrat censuses. F-M = February to March.

s 3926 l

a 4000 4725 u 5000 4180 d

i Revista Brasileira de Ornitologia, 24(2), 2016 v i

s 3926 d l 3000 n a

i 4000

u f 3000 4180 d o i

v r i

e 2000 d 3000 n

i 2000

m b

f 3000 u o

N 1000 r

e 2000 2000 m b

u 0

N 1000 Apr.1982 Mar.1995 1995 1996 Aug.2011 0 Apr.1982 Mar.1995 1995 1996 Aug.2011 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization 103 Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

individuals). This is a conservative estimate, as the species Census standardization proposal breeds in small colonies in high places and areas facing the ocean. In Martin Vaz, several hundred individuals In order to obtain reliable data for long-term monitoring breed, and there is no previous estimate for the island. of seabird populations in the Brazilian islands, a range of Overall, considering every island and species as a methods in different periods of the year should be used. population, of the 35 breeding populations, trends seems Nest mapping methodology is suggested as appropriate upward for 14%, decreasing for 11%, stable for 23%, for Audubon's Shearwater, tropicbirds, Trindade unknown or not possible to evaluate for 49% (Table Petrel, Red-footed Booby, Great Frigatebird and Lesser 3). The Red-footed Booby population from Trindade Frigatebird, while other species populations should be Island is now extinct, and six others, the Lesser and Great by counting nests. The only exceptions are high density Frigatebirds, the Black Noddy from Martin Vaz, the colonies, such as for Sooty Tern in Trindade Island and Audubon's Shearwater and Red-billed Tropicbird from Atol das Rocas, which the most appropriate census is Fernando de Noronha, and the White-tailed Tropicbird random quadrats (100 × 100 m). A summary of methods from Abrolhos, are very tiny, with a real risk of extinction and periods most suitable for censuses is presented in in the short-term. Table 4.

TABLE 4. Recommendation of the most suitable census methodology and breeding periods for seabird counting on Brazilian oceanic islands aiming the standardization and long-term monitoring. SPSPA = São Pedro and São Paulo Archipelago.

Fernando de Trindade and Breeding species SPSPA Atol das Rocas Abrolhos Noronha Martin Vaz Islands Nest mapping1/ Pterodroma arminjoniana - - - - Counting in flight for index locations Puffinus lherminieri - Nest mapping5 - - - Phaethon aethereus - Nest mapping1 - Nest mapping1 - Phaethon lepturus - Nest mapping1 - Nest mapping1 - Sula dactylatra - Counting nests1 Counting nests1 Counting nests1 Counting nests7 Sula leucogaster Counting nests1 Counting nests1 Counting nests1 Counting nests1 - Sula sula - Counting nests1 Counting individuals1* - Fregata magnificens - Counting nests5 Counting individuals1* Counting nests1 - Fregata ariel trinitatis - - - - Counting in flight1 Fregata minor nicolli - - - - Counting in flight1 Anous minutus Counting nests2 Counting nests3 Counting nests1 - Counting nests8 Anous stolidus Counting nests2 Counting nests1 Random quadrats1 Counting nests6 Counting nests8 Gygis alba - Counting nests1 - - Counting nests9 Onychoprion fuscatus - Counting nests4 Random quadrats1 Counting nests6 Random quadrats7 1= whole year, 2 = April to September, 3 = March to August, 4 = August to December, 5 = May to November, 6 = February to September, 7 = October to January, 8 = September to March, 9 = June to December. * Non-breeding at this site.

DISCUSSION Noronha and Trindade/Martin Vaz Islands, remain unknown. In Fernando de Noronha, seabird populations Seabird population trends are distributed in and around the main island, and in 21 adjacent islands and islets (Schulz-Neto 2004) difficult to Population trends of seabirds in Brazil were previously reach. In the main island, species such as the Red-footed unknown, despite the fundamental need for them to Booby, Black Noddy, tropicbirds, and the White Tern produce the Brazilian Red List of Threatened Fauna, nest on trees, cliffs and in rocky crevices of limited access. in 2003 and 2014 (MMA 2014). However, population Moreover, the adjacent islands may become inaccessible trends of about half of the seabird populations breeding due to limited opportunity for landing. Similar access in oceanic islands in Brazil, especially at Fernando de difficulties are also in Trindade/Martin Vaz Islands.

Revista Brasileira de Ornitologia, 24(2), 2016 Revista Brasileira de Ornitologia, 24(2), 2016 104 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

The Sooty Tern is the most abundant seabird in trend estimates, particularly for tropical species for which Brazil, mainly due to its huge colony at Atol das Rocas, seasonality is sometimes limited. Furthermore, the lack of although it is also the most abundant species in Trindade standardized methodology for censuses limits the strength Island as well. On the other hand, Brown Noddy is of estimates of population size and trends. the most widespread species in the offshore islands Seasonal variations in population may occur due to occurring in all five study places. However, considering differences in breeding time between species, as noddies the species breeding on coastal islands, Brown Boobies in SPSPA and Abrolhos breed between March and and Magnificent Frigatebirds are the most widespread September (Alves et al. 1997, Both & Freitas 2004), while species, breeding from Santa Catarina state (~27°S) north Brown Boobies breed throughout the year at SPSPA (Both to SPSPA and Fernando de Noronha, respectively (Sick & Freitas 2004). Thus, knowing the breeding period or 1997). the breeding peak and conducting censuses in comparable Our results indicated that in recent decades there periods is important in order to avoid misinterpretations. was a single local extinction, the Red-footed Booby in This is the reason why we suggested, when possible, Trindade Island. However, there are colonies of only a the most suitable period to carry out census according few individuals of other species, such as the Audubon's to seabird species and breeding site, although such Shearwater and Red-billed Tropicbird in Fernando de information is still lacking for some species and islands. Noronha, White-tailed Tropicbird in Abrolhos, Black Furthermore, the population size may oscillate between Noddy in Martin Vaz, and Great and Lesser Frigatebirds in years and within years due to climatic or environmental Trindade. Thus, local extinctions in the near future would factors affecting prey availability and seabird abundance not be surprising. Trindade/Martin Vaz holds important near breeding areas (Furness & Camphuysen 1997, breeding sites for the endemic subspecies of the Great and Quillfeldt & Masello 2013). The annual seasonal cycles of Lesser Frigatebirds, as well as the only breeding site in seabirds account for much of the total temporal variability the Atlantic Ocean for the Trindade Petrel (Carboneras of populations in all ecosystems (Furness & Camphuysen et al. 2014, Orta et al. 2014b,c). Both frigatebirds have 1997). Although the general seasonal pattern repeats each global populations estimated from 100,000 to 1,000,000 year, climatic variability in the atmosphere and the ocean individuals (Birdlife International 2015) over a broad can generate detectable changes in intensity and onset range, and thus are considered not globally threatened, timing among years and time scales. Consequently, long- but the geographically isolated populations at Trindade term studies are desirable. Island are potentially full species under severe risk of Censuses must be carried out following the same extinction (Olson 1981). Information on the population methodology wherever possible for future comparisons. size in these sites is scarce (Fonseca-Neto 2004) compared For some species, such as the Brown Noddy, there to the other oceanic islands, and more efforts are needed were three different methodologies used for censuses to improve it. Since 2007, a scientific research program at (estimation, direct counting, and random quadrats) Trindade Island (PROTRINDADE) has been designed making some of the data not comparable. Whenever to manage the development of scientific research in the possible, counting the number of breeding pairs or active Trindade/Martin Vaz Islands and the adjacent marine nests (with eggs or chicks) in a given breeding season for a area. Thus, it is expected that in the near future a dataset given species is the most reliable way (Hutchinson 1979, similar to those now available for SPSPA will appear. see Table 4) to provide datasets for different years. This Overall, a monitoring program of seabird should be pursued by different teams and institutions populations based on standardized censuses must be in Brazil working within the same islands over several established to generate a long-term database, enabling decades. However, this is not always possible for numerous population trend analysis and the study of factors that reasons, including the inaccessibility of islands and cliffs, may impact these populations, such as climate change logistics, and the unpredictability of funds, which makes and pollution. Essentially, for all Brazilian oceanic islands it impossible to monitor populations yearly. For these there is an urgent need for seabird population monitoring cases, other methodologies would be useful, as the use of with methodologies that allow more comparable temporal unmanned aerial vehicles to take pictures of colonies (Vas sequences. et al. 2015) or predictive habitat modelling (Scott et al. 2009). Censuses can be undertaken on-board boats along Methodological caveats the coast using sectors marked every kilometer along the perimeter of the island, as well as transects and distance Seabird population trends can only be estimated based sampling (Camphuysen et al. 2004). In Atol das Rocas, on prior counting data (Bibby et al. 1998), and caution there are high population densities of the Sooty Tern must be taken with censuses that do not coincide with and Brown Noddy, which make direct counting very annual peaks in abundance, which affect population laborious. Alternatively, prior studies used the random

Revista Brasileira de Ornitologia, 24(2), 2016 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization 105 Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

quadrat methodology (Antas 1991, Schulz-Neto 1998), endemic frigatebirds, but in 2005 goat eradication was which divided the study site with a grid (either on a map concluded by the Brazilian Navy (Luigi et al. 2009), while or actually on the ground with markers) and used random pigs were eliminated earlier, during the 1950s. The current coordinates to position the sampling site within each grid threat is the introduced House Mouse. Currently, in square, with further extrapolation for the whole area Brazil the Red-footed Booby breeds only in Fernando de (Bibby et al. 1998). However, the extrapolation should Noronha (Fonseca-Neto 2004) and the arboreal breeding be “calibrated” in relation to population density, which habits protected the species of terrestrial predators such makes this methodology rather subjective. Censuses also as (Rattus rattus, R. norvegicus), Tegu Lizard (Salvator should be regularly carried out in the same areas as long merianae) and feral cats (Felis catus) (Barbosa-Filho et al. as they cover all or most of the breeding colonies. For 2009). However, alien predators occur in most of the five cryptic species, such as the burrowing nester Audubon's sites studied. In Fernando de Noronha, potential and Shearwater, whose Brazilian population is small, one chick predators include the Tegu Lizard, rats, cats, pigs, alternative is the use of independent acoustic recording and dogs (Canis familiaris), as well as others that destroy devices, which can be deployed on remote islands to the vegetation, such as the Rock Cavy (Kerodon rupestris), record the vocal activity of seabirds (Buxton & Jones House Mice, and goats (Schulz-Neto 2004). 2012, Buxton et al. 2013, Oppel et al. 2014), or burrow- Another growing threat to these birds is tourism. scopes (e.g. Hamilton 2000). Overall, agreement on the Seabird colonies are valuable tourist attractions, but best way to monitor seabirds in Brazilian islands can only species have different sensitivities to human disturbance be achieved after a thorough discussion among different and their presence in poorly managed sites may negatively research teams, and would potentially be applicable case affect breeding birds (Yorio et al. 2001, Croxall et al. by case, i.e. defining methods specific to each species 2012). Plastic ingestion and oil pollution are also potential and colony/island, for which a first step is provide in the threats (Croxall et al. 2012). Finally, considering recent current study (Table 4). pathogen transmission dynamics due to globalization and climate change (Morse 1995, Altizer et al. 2013), Threats for Brazilian seabirds in breeding grounds infectious diseases also have to be considered as important threats to birds breeding in colonies, since they have All Brazilian offshore islands are now protected areas the potential to cause rapid declines and extinction of under Brazilian legislation. This scenario would guarantee vulnerable populations (Heard et al. 2013). Furthermore, a safe ground for breeding seabirds. However, in the past, storms and pronounced maritime oscillations covering seabird species were threatened by the collection of eggs the marginal areas of an archipelago are natural causes of and nestlings, hunting, habitat degradation, and the population decrease. In SPSPA, waves carried away eggs introduction of alien invasive predators (Antas 1991, Alves and nestlings in October 1999 (Both & Freitas 2004) and et al. 2004, Fonseca-Neto, 2004, Schulz-Neto 2004), and June 2014 (G. T. Nunes and F. P. Marques, pers. comm.). some threats are still affecting their populations. All of the above threats, natural and anthropogenic, Seabird hunting and the collecting of eggs and are ongoing in Brazilian seabird populations within nestlings are forbidden by law (Law of Environmental offshore islands. Nevertheless, without knowing the Crimes No. 9605/98), but in the past these activities real population sizes and monitoring them through might have been responsible for population declines standardized censuses, it will be difficult to take effective for some species, such as tropicbirds in Fernando de actions for conservation purposes. We reinforce the urgent Noronha, usually used as food and handcrafts (Nacinovic need for additional studies focusing on rigorous and & Teixeira 1989). In 1870, when Fernando de Noronha standardized methods for seabird population estimations, was a penal colony, almost all vegetation was removed to using comparable temporal methodologies. avoid prisoner escape, which caused the tree-nesting Red- footed Booby to disappear from the island for a time (Oren 1984, Antas 1991, Schulz-Neto 2004). For centuries, ACKNOWLEDGEMENTS egg collecting and the poaching of adults was a common practice, as well described at SPSPA and Abrolhos by We thank Fernanda P. Marques, Guilherme T. Nunes, Darwin during his voyage on the Beagle (Darwin 2008). Felipe M. Neves, Luciana R. Camillo, Vivian L. Ferreira, In Trindade Island, the forests historically covered 85% of Isaac Simão Neto, Andrei L. Roos, Wolgrand M. Falcão, the island, but decreased to less than 5% due to devastation Márcio A. Efe and Gustavo R. Leal for assistance in by feral pigs (Sus scrofa), goats (Capra hircus), House Mice fieldwork. Thanks also to ICMBio and Fernando de (Mus musculus), and fire (Alves 1998). Habitat alteration Noronha Administration for logistic support during critically reduced nesting opportunities for tree-nesting Fernando de Noronha expeditions, and Zelinha Britto seabirds such as the Red-footed Booby and the two at REBIO Atol das Rocas. Brazilian Navy and Comissão

Revista Brasileira de Ornitologia, 24(2), 2016 Revista Brasileira de Ornitologia, 24(2), 2016 106 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni

Interministerial para os Recursos do Mar (CIRM/SECIRM) Bugoni, L. & Vooren, C. M. 2005. Distribution and abundance of for logistic support for the Trindade and SPSPA six tern species in southern Brazil. Waterbirds, 28: 110–119. Buxton, R. T. & Jones, I. L. 2012. Measuring nocturnal seabird expeditions, and the Brazilian Research Council (CNPq activity and status using acoustic recording devices: applications - Grant No. 557152/2009-7) for funding the project. for island restoration. Journal of Field Ornithology, 83: 47–60. P.L.M. acknowledges CAPES Foundation for providing Buxton, R. T.; Major, H. L.; Jones, I. L. & Williams, J. C. 2013. grant No. 9733/2011-6. PLM is a postdoctoral fellow of Examining patterns in nocturnal seabird activity and recovery the Fundação de Amparo à Pesquisa do Estado de São Paulo across the western Aleutian Islands, Alaska, using automated acoustic recording. Auk, 130: 331–341. (Proc. No. 2014-00194-2). L.B. is a research fellow from Camphuysen, K. C. J.; Fox, T. A. D.; Leopold, M. M. F. & Peterson, the Brazilian CNPq (Proc. No. 310550/2015-7). Authors I. K. 2004. Towards standardised seabirds at sea census techniques in are grateful to four reviewers which greatly improved connection with environmental impact assessments for offshore wind earlier versions. farms in the U.K. Amsterdam: Royal Netherlands Institute for Sea Research. Carboneras, C.; Jutglar, F. & Kirwan, G. M. 2014. Audubon's Shearwater (Puffinus lherminieri). In: del Hoyo, J.; Elliott, A.; REFERENCES Sargatal, J.; Christie, D. A. & Juana, E. (eds.). Handbook of the birds of the world alive. Barcelona: Lynx Edicions. http://www. Altizer, S.; Ostfeld, R. S.; Johnson, P. T. J.; Kutz, S. & Harvell, D. hbw.com/node/52580 (access on 28 October 2014). 2013. Climate change and infectious diseases: from evidence to a Coelho, A. G. M. 1981. Observações sobre a avifauna do Arquipélago predictive framework. Science, 341: 514­­­–519. dos Abrolhos, Bahia. 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Revista Brasileira de Ornitologia, 24(2), 2016 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization 109 Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni slands i slands i slands i - Flying Remarks slands and Ponta da Sapata slands and Ponta i and Siriba and Siriba Ponta das Caracas Ponta Chapéu, Rasa Morro da Viuvinha Island Viuvinha da Morro Morro da Viuvinha Island Viuvinha da Morro Morro da Viuvinha Island Viuvinha da Morro Morro da Viuvinha Island Viuvinha da Morro Morro da Viuvinha Island Viuvinha da Morro Island Viuvinha da Morro juveniles found at the beach juveniles juveniles found at the beach juveniles juveniles found at the beach juveniles Sta. Barbara, Sueste, Guarita,. Redonda, Redonda, Guarita,. Sueste, Barbara, Sta. Chapéu, Rasa Morro da Viuvinha and Morro do Leão and Morro Viuvinha da Morro References Oren (1982) Oren (1984) Oren Antas (1991) Antas (1991) Present study Present Present study Present study Present Present study Present Present study Present study Present Brooke (2004) Brooke in Nunes 2012 in Nunes CEMAVE data CEMAVE data CEMAVE Martins (2004) Martins (in Nunes 2012) (in Nunes Alves et al. (1997) Alves Luigi et al. (2009) Luigi Silva-e-Silva (2008) Silva-e-Silva (2008) Silva-e-Silva (2008) Silva-e-Silva (2008) Silva-e-Silva Mestre et al. (2009) Mestre Schulz-Neto (2004) Schulz-Neto Efe unpublished data Efe Fonseca-Neto (2004) Fonseca-Neto Sarmento et al. (2014) Sarmento Soto & Filipini (2001) & Filipini Soto Soto & Filipini (2001) & Filipini Soto Soto & Filipini (2001) & Filipini Soto Nacinovic et al. (1989) Nacinovic M. A. Efe (unpublished data) M. A. Efe Silva-e-Silva & Olmos (2010) & Olmos Silva-e-Silva Silva-e-Silva & Olmos (2010) & Olmos Silva-e-Silva Silva-e-Silva & Olmos (2010) & Olmos Silva-e-Silva Estimation Methods Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct counting Direct counting Direct counting Direct Direct counting Direct counting Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Estimation (unexplained guess) APPENDIX I APPENDIX Direct counting, mapping nest+estimation Direct 2011 2003 2004 2005 2008 July 2011 July June 1992 June April 1981 April April 2011 April 1989 – 2000 2011 – 2012 1994 – 2000 August 1990 August August 2011 August August 2010 August August 2010 August August 1988 August October 2005 October February 2011 February Month/Year December 1982 December November 1991 November November 2004 November November 2011 November 2010 November September 2003 September September 1993 September April 2003 – April March April 2006 – April January January 1987 – 1995 January January 2012 2011 – January August October 2005 and September 2006 2005 and September October ------1 6 2 2 8 3 7 4 1 40 11 50 70 31 10 13 99 269 102 No. No. 1130 Nests 4 2 4 7 2 5 4 7 4 6 5 1 8 2 80 30 12 62 30 22 10 14 26 100 140 538 709 204 198 No. No. 6500 2000 15,000 3000 – 5000 Individuals Island Fernando de Fernando de Fernando de Fernando Abrolhos Arch. Arch. Abrolhos Noronha Arch. Arch. Noronha Arch. Noronha Arch. Noronha Trindade Island Trindade Archipelago/ Species Pterodroma arminjoniana Puffinus lherminieri Phaethon aethereus Phaethon lepturus Bibliographic revision and new data on population estimates of seabirds breeding on Brazilian offshore islands. offshore on Brazilian breeding and new data on population estimates of seabirds revision Bibliographic

Revista Brasileira de Ornitologia, 24(2), 2016 Revista Brasileira de Ornitologia, 24(2), 2016 110 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni slands i slands i slands i slands slands slands slands i i i i sland slands i i slands slands i i Remarks Rasa Island MeioIsland Whole Island External External External External Martin Vaz Vaz Martin Rata, Meio Rata, Meio Sta. Barbara Island Barbara Sta. Rata, Rasa Meio Rata, Rasa Meio Rata, Rasa Meio Rata, Rasa Meio Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Rata (80), Meio (360) Islands Rata (80), Meio Rata (50), Ovos (120) Islands Rata (50), Ovos Redonda, Siriba, Sueste Sueste Siriba, Redonda, (active search) = 124 individuals search) (active flying or resting (onboard census) resting (onboard flying or Redonda, Siriba, Sueste, Sta. Barbára Barbára Sta. Sueste, Siriba, Redonda, 120 flying or resting (onboard census) and 62 nests resting (onboard 120 flying or Meio (180), Ovos (70), Rata and Macaxeira (25) (70), Rata and Macaxeira (180), Ovos Meio References Oren (1984) Oren Antas (1991) Antas (1991) Antas (1991) Antas (1991) Antas (1991) Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Martins (2004) Martins Martins (2004) Martins Alves et al. (2000) Alves Alves et al. (2004) Alves Kohlrausch (2003) Kohlrausch Silva-e-Silva (2008) Silva-e-Silva Silva-e-Silva (2008) Silva-e-Silva Silva-e-Silva (2008) Silva-e-Silva Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (2004) Schulz-Neto Schulz-Neto (2004) Schulz-Neto Fonseca-Neto (2004) Fonseca-Neto Present study (CEMAVE) Present Present study (CEMAVE) Present Present study (CEMAVE) Present Methods Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Randon quadrats Randon quadrats Randon quadrats July 1994 July July 2011 July June 2002 June June 1987 June June 2013 June April 2007 April April 1991 April April 1991 April 2000 -2002 March 2011 March August 2011 August August 2000 August August 2010 August August 2011 August August 2010 August January 1992 January January 2012 January August 2010 August October 1999 October October 1987 October February 2011 February February 1982 February February 1990 February February 2011 February February 2008 February Month/Year December 1988 December December 1982 December November 1991 November November 1991 November November 2010 November November 2010 November September 1994 September April 2003 – April March April 2003 – April March March 2012 – March February October 2010 – October September August 1994 to April 2000 1994 to April August April 2007 2006 – April December ------2 1 5 38 72 62 800 825 486 275 275 281 321 131 200 120 No. No. 3175 Nests 5 7 2 53 70 18 600 123 150 160 287 550 440 170 420 175 450 200 100 105 600 546 244 300 262 400 588 No. No. 1600 1850 1591 5000 4000 1600 5100 6400 1600 2072 1248 Individuals Island Fernando de Fernando & Vaz Martin São Pedro and Pedro São Atol das Rocas Atol Abrolhos Arch. Arch. Abrolhos Abrolhos Arch. Arch. Abrolhos Noronha Arch. Arch. Noronha Trindade Island Island Trindade São Paulo Arch. Arch. Paulo São Archipelago/ Sula dactylatra Sula Sula leucogaster Sula Species

Revista Brasileira de Ornitologia, 24(2), 2016 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization 111 Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni slands i slands slands i i slands i slands slands slands slands slands slands slands slands slands slands slands i i i i i i i i i i i slands slands i i Port Remarks Sueste Island Sueste External External External External Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Cemitério, Farol Redonda, Siriba and Sueste and Sueste Siriba Redonda, Sela Gineta, Meio Islands and Caieiras Islands Meio Gineta, Sela Port, Meio, Viuvinha, Cabeluda Viuvinha, Meio, Port, Port, Meio, Viuvinha, Cabeluda Viuvinha, Meio, Port, Breed in all islands, except Principal and Rasa Principal in all islands, except Breed Redonda, Siriba, Sueste and Sta. Barbára Barbára and Sta. Sueste Siriba, Redonda, References Antas (1991) Antas (1991) Antas (1991) Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Masch (1966) Masch Coelho (1981) Martins (2004) Martins et al. (2000) Alves Kohlrausch (2003) Kohlrausch Kohlrausch (2003) Kohlrausch Smith et al. (1974) Smith Mackinnon (1962) Mackinnon Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (2004) Schulz-Neto Schulz-Neto (2004) Schulz-Neto Edwards et al. (1981) Edwards Both & Freitas (2004) Both & Freitas Both & Freitas (2004) Both & Freitas Present study (CEMAVE) Present Present study (CEMAVE) Present Barbosa-Filho & Vooren (2010) Vooren & Barbosa-Filho Barbosa-Filho & Vooren (2010) Vooren & Barbosa-Filho Estimation Methods Linear quadrats Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Randon quadrats Randon quadrats Direct counting / Estimation Direct 1969 2001 June 2013 – June July 1994 July July 2011 July June 2002 June May 1971 May May 1989 May May 2014 May April 1991 April April 1991 April April 2011 April 1999/2000 1999 – 2000 2000 – 2002 March 2011 March March 1966 March August 2011 August August 2010 August August 2011 August August 2010 August January 2012 January October 2010 October February 2011 February February 1982 February February 1990 February February 1990 February Month/Year May November 1991 November November 1991 November November 1991 November November 2010 November November 1960 November September 1994 September September 1994 September September 1979 September July 2002 – July March April 2003 – April March February / March 2012 / March February November 2001 – November September ------93 29 64 35 115 230 100 155 160 No. No. Nests 3 4 8 1 9 7 3 1 76 80 34 81 98 80 66 61 230 400 460 186 200 300 300 300 250 350 125 152 269 870 163 500 200 439 500 330 200 377 381 No. No. Individuals Island Fernando de Fernando São Pedro and Pedro São Atol das Rocas Atol Abrolhos Arch. Arch. Abrolhos Noronha Arch. Arch. Noronha São Paulo Arch. Arch. Paulo São Archipelago/ Sula sula Sula Species

Revista Brasileira de Ornitologia, 24(2), 2016 Revista Brasileira de Ornitologia, 24(2), 2016 112 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni slands slands i i Remarks Redonda Island Redonda Redonda Island Redonda Redonda Island Redonda Principal Island Principal Redonda Island Redonda Individuals flying Individuals Sela Gineta Island Gineta Sela Island Gineta Sela Sela Gineta Island Gineta Sela Sta. Barbara Island Barbara Sta. No breeding record. breeding No Onboard, external Onboard, Onboard, external Onboard, Farol Island (Coconut tree) Island Farol After intensive search. Probably extinct. Probably search. After intensive Farol Island (Coconut tree), 9 adults, 33 juveniles (Coconut tree), Island Farol References Luigi (1992) Luigi Oren (1984) Oren Oren (1984) Oren Antas (1991) Antas (1991) Antas (1991) Antas (1991) Antas (1991) Present study Present Present study Present Present study Present Present study Present study Present study Present Present study Present Present study Present study Present Present study Present Present study Present Olson (1981) Olson Olson (1981) Olson Martins (2004) Martins et al. (1997) Alves et al. (1997) Alves Schulz-Neto (1998) Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto (1998) Schulz-Neto Schulz-Neto (2004) Schulz-Neto Fonseca-Neto (2004) Fonseca-Neto Present study (CEMAVE) Present Present study (CEMAVE) Present Present study (CEMAVE) Present Present study (CEMAVE) Present Schulz-Neto (1995, 2004) Schulz-Neto Barbosa-Filho & Vooren (2009) Vooren & Barbosa-Filho Methods Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct counting Direct Direct counting Direct counting Direct Direct counting Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Randon quadrats Photographs, estimated based on Photographs, - 1982 1987 late 1980 July 2011 July June 1987 June April 1991 April April 1991 April 1975-1976 March 1994 March August 2011 August August 2010 August August 2010 August October 1994 October February 2011 February February 2011 February February 1982 February 1982 February Month/Year December 1982 December November 1991 November November 1991 November November 1992 November November 2010 November November 2010 November September 1994 September 1994 September September 2010 September April 2003 – April March April 2011 – April March March 2012 – March February March 2012 – March February August 1994-April 2000 1994-April August November 1991 – November October October 2010 – October September November – November and October – June April/July / November 2008 / November April/July April 2007 2006 – April December April 2007 2006 – April December January 1976 1975 – January December May ------0 60 15 115 166 427 330 100 215 No. No. 1290 Nests 1 7 4 2 0 50 50 20 40 12 15 30 87 50 120 230 332 854 660 100 201 300 200 253 200 350 430 150 733 122 No. No. 4000 1658 2580 1513 1184 1882 1440 1511 Individuals Island Fernando de Fernando de Fernando & Vaz Martin & Vaz Martin Atol das Rocas Atol Atol das Rocas Atol Abrolhos Arch. Arch. Abrolhos Arch. Abrolhos Noronha Arch. Arch. Noronha Arch. Noronha Trindade Island Island Trindade Trindade Island Island Trindade Archipelago/ Fregata ariel Fregata trinitatis Fregata Fregata magnificens Species

Revista Brasileira de Ornitologia, 24(2), 2016 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization 113 Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni slands i slands i Remarks Principal Island Principal Viuvinha Island Viuvinha Whole Archipelago Whole Archipelago Whole Archipelago Whole Archipelago Whole Archipelago Whole Archipelago Whole Archipelago Whole Archipelago No breeding record breeding No No breeding record breeding No Viuvinha Island, Port, Island, Viuvinha Sancho Bay to Ponta da Sapata to Ponta Bay Sancho Farol (1100), Cemitério (380) Farol Mirante dos Golfinhos and São José São and dos Golfinhos Mirante Farol Island (Coqueiros and Scientific station) (Coqueiros Island Farol Following a fishing vessel near Ponta Noroeste Ponta vessel near a fishing Following Sancho Bay to Ponta da Sapata and Viuvinha Island Viuvinha and da Sapata to Ponta Bay Sancho Norte Island, Martin Vaz. Nest content not checked. Nest Vaz. Martin Island, Norte References Oren (1984) Oren Oren (1984) Oren Antas (1991) Antas (1991) Antas (1991) Antas (1991) Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present study Present Present study Present Olson (1981) Olson Martins (2004) Martins Martins (2004) Martins Smith et al. (1974) Smith Smith et al. ( 1974) Smith Mackinnon (1962) Mackinnon Mackinnon (1962) Mackinnon Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto (1998) Schulz-Neto Edward et al. (1981) Edward Edward et al. (1981) Edward Fonseca-Neto (2004) Fonseca-Neto Both & Freitas (2004) Both & Freitas Both & Freitas (2004) Both & Freitas Both & Freitas (2004) Both & Freitas Both & Freitas (2004) Both & Freitas Both & Freitas (2004) Both & Freitas plumages Estimation Estimation Estimation Estimation Methods Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Randon quadrats Randon quadrats Direct counting/estimation Direct Randon quadrats/direct counts Randon quadrats/direct Photographs, estimated based on Photographs, July 2011 July July 2011 July May 1971 May June 1987 June May 1989 May May 1971 May April 2011 April April 2007 April April 2007 April April 2000 April 1999 – 2000 1975 – 1976 1999 – 2000 March 2011 March August 2010 August 2010 August October 2010 October October 1987 October October 2010 October February 1993 February February 1982 February Month/Year December 1982 December December 1982 December November 1960 November November 1960 November September 1994 September September 1979 September September 1979 September August 2000 – August July August 2000 – August July April 2003 – April March April 2003 – April March March 2012 – March February March 2012 – March February April / November 1991 / November April April 2000 1994 – April August April 2007 2006 – April December ------6 9 10 30 15 110 162 No. No. Nests 10,630 1 3 90 30 220 604 160 ~20 480 200 886 213 498 387 300 490 165 390 120 150 481 366 320 220 300 324 No. No. 4039 2000 3192 2000 1750 1750 5000 1480 18,700 21,260 Individuals Island Fernando de Fernando Fernando de Fernando & Vaz Martin & Vaz Martin São Pedro and Pedro São and Pedro São Atol das Rocas Atol Atol das Rocas Atol Noronha Arch. Arch. Noronha Noronha Arch. Arch. Noronha Trindade Island Island Trindade Trindade Island Island Trindade São Paulo Arch. Arch. Paulo São Arch. Paulo São Archipelago/ Species minor Fregata nicoli minutus Anous stolidus Anous

Revista Brasileira de Ornitologia, 24(2), 2016 Revista Brasileira de Ornitologia, 24(2), 2016 114 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni slands i slands i Paredão Farilhões Remarks Praia do M Praia Racha Island Pico Pico do Vigia Pão de Açúcar Pão Guarita Island Guarita Guarita Island Guarita Guarita Island Guarita Guarita Island Guarita Guarita Island Guarita Praia Noroeste Praia Viuvinha Island Viuvinha Pico Monumento Pico Praia das Cabritas Praia Whole Trindade Is. Whole Trindade Whole Trindade Island Whole Trindade near Pico Pão de Açúcar Pão near Pico Viuvinha, São José José São Viuvinha, Martin Vaz (nests with eggs) Vaz Martin Crista do Galo & Ponta Norte & Ponta do Galo Crista Pico Nossa Senhora de Lourdes Senhora Nossa Pico On board around the Principal Island the Principal around board On On board around the Principal Island the Principal around board On Whole archipelago (mainly Principal Is.) (mainly Principal Whole archipelago Baía dos Porcos to Mirante dos Golfinhos / Morro do Piquinho do Morro / dos Golfinhos to Mirante dos Porcos Baía Piquinho do Morro / dos Golfinhos to Mirante dos Porcos Baía Viuvinha, Cuzcuz, Morro do Leão, Morro da Viuvinha Viuvinha da do Leão, Morro Morro Cuzcuz, Viuvinha, References Oren (1984) Oren Antas (1991) Antas (1991) Antas (1991) Present study Present study Present study Present Present study Present study Present study Present Present study Present study Present Present study Present Present study Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present study Present Present study Present Present study Present Martins (2004) Martins Murphy (1936) Murphy Alves et al. (2000) Alves Schulz-Neto (1998) Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Fonseca-Neto (2004) Fonseca-Neto Fonseca-Neto (2004) Fonseca-Neto Fonseca-Neto (2004) Fonseca-Neto Fonseca-Neto (2004) Fonseca-Neto Present study (CEMAVE) Present Counting Counting Estimation Estimation Estimation Estimation Estimation Estimation Methods Direct counting Direct Direct counting Direct counting Direct counting Direct Direct counting Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Direct counting Direct Randon quadrats Randon quadrats Randon quadrats Randon quadrats Randon quadrats Direct counting+Estimation Direct ? 1995 1996 July 2011 July July 2011 July April 2007 April April 2011 April April 1982 April April 1991 April 1994 – 2000 March 1995 March March 1979 March March 2011 March August 2011 August August 2010 August October 1987 October February 1982 February February 1990 February Month/Year December 2006 December 2006 December December 2006 December December 2006 December December 1982 December November 1991 November April 2003 – April March March 2007 – March January March 2007 – March January March 2007 – March January 2007 – March January March 2007 – March January March 2007 – March January March 2007 – March January November 1987 – November June August 2010 (CEMAVE) August August 1994 to April 2000 1994 to April August April 2007 2006 – April December November 2010 (CEMAVE) November March 2007 2006 – March December ------5 1 3 3 8 20 88 40 10 20 30 42 15 No. No. ~250 1000 1200 1275 1120 Nests 40 30 50 82 62 800 120 250 133 310 325 400 252 No. No. >500 2000 3000 3926 4180 2400 4725 1000 2240 > 500 10,000 17,700 27,390 11,800 Individuals Island Fernando de Fernando Fernando de Fernando & Vaz Martin & Vaz Martin Abrolhos Arch. Arch. Abrolhos Noronha Arch. Arch. Noronha Noronha Arch. Arch. Noronha Trindade Island Island Trindade Trindade Island Island Trindade Archipelago/ Onychoprion Onychoprion fuscatus Gygis alba Gygis Species

Revista Brasileira de Ornitologia, 24(2), 2016 Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization 115 Patrícia L. Mancini, Patrícia P. Serafini and Leandro Bugoni sland i Remarks Martin Vaz Martin Whole Island Whole Guarita Island Guarita Guarita Island Guarita Guarita Island Guarita elsewhere <1000 pairs elsewhere main concentration of 450 eastern end the island, References Antas (1991) Antas (1991) Antas (1991) Present study Present Present study Present Present study Present Present study Present Present study Present Present study Present Olson (1981) Olson Alves et al. (2000) Alves Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Schulz-Neto (1998) Schulz-Neto Fonseca-Neto (2004) Fonseca-Neto Methods Direct counting Direct Direct counting Direct Direct counting Direct Randon quadrats Randon quadrats Randon quadrats Randon quadrats Randon quadrats Randon quadrats Randon quadrats Randon quadrats Partial counts+estimation Partial August 1994 to April 2000 1994 to April August Direct counting+estimation Direct feathers and abandoned colonies ? April 2007 April April 1991 April 1994 – 2000 March 1979 March August 2011 August October 2010 October February 1982 February February 1990 February February 1993 February Month/Year November 1991 November March 2012 – March February March 2007 2006 – March December February 1976 1975 – February December ------20 No. No. 1450 2924 Nests 40 10 10 No. No. 4000 2900 6000 30,000 40,000 75,000 15,846 28,956 115,000 106,620 140,000 Individuals several hundreds several Island & Vaz Martin Atol das Rocas Atol Abrolhos Arch. Arch. Abrolhos Trindade Island Island Trindade Archipelago/ Species

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