Bugoni & Furness: Age composition and sexual size dimorphism of albatrosses and 253

AGE COMPOSITION AND SEXUAL SIZE DIMORPHISM OF ALBATROSSES AND PETRELS OFF BRAZIL

LEANDRO BUGONI1,2 & ROBERT W. FURNESS1

1Faculty of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow, G12 8QQ, UK 2Current address: UFPel, Instituto de Biologia, Campus Universitário Capão do Leão, CP 354, 96010-900, Pelotas, RS, Brazil ([email protected])

Received 18 May 2008, accepted 25 August 2009

SUMMARY

BUGONI, L. & FURNESS, R.W. 2009. Age composition and sexual size dimorphism of albatrosses and petrels off Brazil. Marine Ornithology 37: 253–260.

We present data on age composition and sexual size dimorphism (SSD) of albatrosses, petrels and in southern Brazil for 301 of 14 captured live at sea. The pelagic community of off Brazil comprises birds of different ages and breeding status according to species. Although juveniles of some species such as Black-browed Albatross Thalassarche melanophris and Southern Giant Macronectes giganteus predominated, all age classes (including breeding birds) were recorded for Atlantic Yellow-nosed T. chlororhynchos and Wandering Diomedea exulans albatrosses. For this heterogeneous community composed of individuals from different colonies, with adults and immature birds pooled, the SSD was more pronounced in bill measurements than in other traits (confirming previous studies) and more conspicuous in giant petrels and Diomedea albatrosses. Closely related species pairs of Thalassarche albatrosses and petrels had differing levels of sexual dimorphism. All linear external traits measured within Thalassarche and Procellaria overlapped considerably and, despite being significantly different, were not adequate for species determination or sexing.

Key words: Sexual size dimorphism, age composition, pelagic community, albatross, petrel

INTRODUCTION sex determination based on linear morphometrics in this mixed stock. Moreover, sexual size dimorphism (SSD) in a pelagic assemblage of Information on some Brazilian species has been obtained seabirds with individuals from varying origins could potentially differ mostly through beached carcasses (Olmos et al. 1995, Martuscelli from SSD measured in colonies, with implications for hierarchy of et al. 1997, Sick 1997, Bugoni et al. 2003, Lima et al. 2004, access to discards from fisheries or prey, and thus play a role in niche Bugoni 2006) or studies focused on incidental capture in fisheries partitioning (Furness et al. 1988, Ballance 2007). (e.g. Neves & Olmos 1997; Olmos et al. 2001; Neves et al. 2007; Bugoni et al. 2008a, 2008c). Few studies have described Of studies on the at-sea component of seabirds’ lives, the the pelagic community at sea through census of birds attending preponderance have been obtained through remote sensing devices bottom longline vessels (Olmos 1997, Olmos & Bugoni 2006) or or ship-based censuses (Ballance 2007). The recent development through snapshot and continuous censuses (Neves et al. 2006). of a non-destructive method for trapping seabirds at sea from Overall, 10 albatross (Diomedeidae) and 31 petrel (, fishing vessels (Bugoni et al. 2008b) allowed us to sample a Hydrobatidae, Pelecanoididae) species have been recorded in range of albatross and petrel species attending vessels. Here, we Brazil (CBRO 2009), with only two species breeding in Brazilian describe the community of pelagic seabirds off Brazil in terms of territory (Trindade Petrel Pterodroma arminjoniana and Audubon’s age composition, and we investigate the SSD of birds sexed by Puffinus lherminieri). The pelagic seabird community molecular methods. in Brazilian waters is generally thought to be composed of • birds that breed elsewhere and migrate to the area during the MATERIALS AND METHODS non-breeding period, Study area and seabird trapping • birds that reach the area during breeding periods when they perform long foraging trips, and Albatrosses and petrels were captured as described by Bugoni • first-year juveniles and older but still immature birds (Neves et et al. (2008b), from vessels using a range of hook-and-line and al. 2006). pelagic longline fishing methods targeting tuna Thunnus spp., sharks (mainly Blue Shark Prionace glauca) and Swordfish Xiphias For some species, birds from different colonies or populations could gladius. This fleet operates in deep waters over the continental shelf potentially occur in the area, which is a further complicating factor for and offshore waters in southern Brazil throughout the year (Mayer

Marine Ornithology 37: 253–260 (2009) 254 Bugoni & Furness: Age composition and sexual size dimorphism of albatrosses and petrels

& Andrade 2005). The main fishing area for this fleet is under the vials preserved with absolute ethanol. Sexing of birds was carried influence of the Subtropical Convergence, formed by the meeting of out after DNA extraction and polymerase chain reaction (PCR) the warm tropical Brazilian Current flowing southward and the cold amplification of CHD genes using primers 2550F (Fridolfsson & Malvinas/Falkland Current flowing northward (Garcia 1998). The Ellegren 1999) and 2757R (R. Griffiths unpub. data) and genes overlap between the fishing fleet and the distribution of albatrosses separated in 2% agarose gel by electrophoresis. Briefly, copies of and petrels is cause for concern because of incidental bycatch of CHD genes are present in both Z and W sexual chromosomes. these seabirds on longline hooks, mainly from June to November CHD-Z and CHD-W genes differ in the base pair length of their (Bugoni et al. 2008c). non-coding regions. Because females are heterogametic (ZW) and males homogametic (ZZ), separation of gene amplification Baits and shark liver were used to attract birds close to the vessel; products by size results in a single band for males and two bands the birds were then captured using a cast net (Bugoni et al. 2008b). for females. DNA extraction negative controls were included for Captures occurred during six cruises and 58 trapping days from every 23 samples. Positive and negative controls were included February to June 2006 and July to September 2007, between for each PCR reaction, and one third of all DNA extractions were 25°S and 35°S. In addition, a few birds incidentally captured in repeated to confirm sex assignment. Furthermore, we used samples hook-and-line fisheries taking place onboard were sampled from of previously sexed birds as controls: February to May, but not in August/September. • One male Atlantic Yellow-nosed Albatross killed in fisheries, sex determined by necropsy and gonad examination Measurements Measurements of birds were taken using Vernier callipers with an • Four ringed Wandering Albatrosses that we sexed, but accuracy of ±0.1 mm and included exposed culmen (= bill) length, subsequently discovered were of known sex from observations at from the bill tip to the point where feathers begin to hide the culmen; the breeding colony (A. Wood & R.A. Phillips, British Antarctic bill depth at the base of the bill; and tarsus (= tarsometatarsus) Survey, in litt.). length, measured from the middle tarsal joint to the distal end of the tarsometatarsus (with foot closed towards tail). Wing chord All control birds were correctly sexed by the molecular method. length, from the carpal joint to the tip of the longest primary feather of the right wing, was taken using a stopped rule; tail length was Data analysis obtained using a metal ruler, from the point at which the longest tail feather emerged from skin, by inserting the rule parallel to the Distribution of the biometric data was inspected graphically to tail feathers. Wing and tail were both measured with an accuracy detect outliers and odd values, which were rechecked against field of ±1 mm, except in birds moulting the outer primaries (no wing datasheets and corrected. Unrealistic values were removed, but measurement taken) or longest tail feathers (no tail measurement some apparent outliers from consistently small or large individuals taken). All measurements were taken by the same researcher (LB) were maintained. Measurements are presented as mean ± one throughout the period. standard deviation and range (minimum and maximum) for males and females. Wandering Diomedea exulans and Tristan D. dabbenena albatrosses are virtually identical in plumage (Onley & Scofield 2007), and so The SSD was calculated for all variables as the ratio between the we used the discriminant function in Cuthbert et al. (2003) to assign average values for females and males. Statistical differences were species. Using culmen length, we further confirmed identification tested by the nonparametric Mann–Whitney test (Fowler et al. after sexing birds by molecular methods (see Cuthbert et al. 2003 1998), which overcomes problems associated with non-normal for details). distribution and heteroscedasticity. Furthermore, we considered that reversed sexual dimorphism (i.e. females larger than males) Ageing could occur, because it is frequent in seabirds (Catry et al. 1999, Bridge 2006, Onley & Scofield 2007). We therefore assumed the Pictures of bills and general plumage were taken from albatrosses same probability of males being larger or smaller than females and giant petrels for ageing. Giant petrels change plumage colour by conducting two-tailed tests (Fowler et al. 1998). Comparison from wholly dark brown to pale brown-greyish with age, which between biometric values of closely related pairs of species was is also used to identify juveniles from older birds. Black-browed carried out to provide support for identification of partial specimens Albatrosses Thalassarche melanophris change bill colour with age, from stranded birds. For this analysis, the Mann–Whitney test was which combined with wing moult, allows for age determination used, and the Bonferroni correction for multiple comparisons was up to six years old (Prince & Rodwell 1994). The same patterns applied; thus, the P value was 0.01. Statistical tests were carried of bill colour changes and moult were described for Grey-headed out using BioEstat software, version 5.0 (Ayres et al. 2007), and Albatrosses T. chrysostoma (Prince & Rodwell 1994). Ageing Minitab Software (version 15.1: Minitab, State College, PA, of Atlantic Yellow-nosed Albatrosses T. chlororhynchos, which USA). change from a wholly dark bill to orange at the culminicorn, ramicorn and ungues (Bugoni & Furness 2009) was used for ageing RESULTS that species. Birds not moulting during or after the breeding season were considered first-year juveniles. We captured a total of 301 birds from 14 species, including nine petrel and shearwater (Procellariidae), four albatross (Diomedeidae) Molecular sexing and one storm-petrel (Procellariidae) species (Table 1). All birds from the 14 species studied were successfully sexed using primers Blood samples (1 mL) were taken by syringe and needle from the 2550F and 2757R. tarsal vein of every bird. Subsamples of blood were stored in 1.5 mL

Marine Ornithology 37: 253–260 (2009) Bugoni & Furness: Age composition and sexual size dimorphism of albatrosses and petrels 255 77 92 134 138 171 184 Tail (n=45) (n=16) (n=25) (n=36) (n=20) 124; 119 206; 191; 201 67.5±2.7; 65–71 99.2±3.4; 93–104 97.4±3.8; 93–104 126±5.9; 119–137 113.9±5.5; 98–122 114.1±4.2; 106–120 127.7±4.7; 117–135 116.4±4.3; 105–125 115.7±4.4; 109–123 111.8±5.6; 100–124 202.3±8.3; 192–212 184.1±8.3; 170–205 195.9±7.3; 186–211 189.2±8.1; 175–201 177.4±4.1; 170–182 168.3±8.1; 160–177 197.3±12.8; 179–215 202.8±11.9; 191–216 — 370 538 289 310 632 (n=6) (n=8) (n=4) (n=0) Wing (n=35) (n=24) (n=32) (n=18) 343; 347 327±5.5; 319–335 374±8.0; 355–392 647±13.6; 627–656 271.6±5.2; 260–278 266.8±7.6; 257–278 393.7±7.1; 380–408 363.2±8.0; 355–376 324.9±7.6; 305–340 325.4±9.7; 305–345 114.3±8.6; 133–151 543.5±9.8; 530–560 525.7±8.6; 513–541 525.3±12.3; 506–548 500.4±15.4; 465–520 490.5±13.3; 475–515 482.8±16.4; 464–497 688.3±13.6; 672–703 389±12.4; 372–413 (9) (mm) a,b 58.5 56.6 55.9 59.6 104.1 111.8 (n=37) Tarsus 52.4; 54.5 112.7; 120.1; 113.9 46.3±1.8; 42.6–50.3 67.3±2.1; 63.7–70.2 66.6±2.4; 62.0–71.0 35.5±1.1; 33.9–36.5 44.5±1.8; 42.0–46.6 66.5±2.5; 63.5–71.6 64.6±1.9; 60.9–67.0 59.0±1.6; 56.2–62.0 49.8±2.2; 46.7–54.2 59.8±2.0; 54.9–64.7 86.1±3.0; 82.2–89.9 83.1±2.8; 77.3–87.1 84.6±2.6; 81.9–88.1 83.6±2.2; 79.8–88.4 78.8±2.0; 74.7–81.7 95.0±4.1; 88.0–101.3 Measurements 115.4±6.0; 107.7–120.3 124.4±1.7; 122.2–126.1 42 19.3 19.4 14.7 14.4 57.4 (n=3) (n=11) 17.7; 15.9 Bill depth 58.6; 60.3; 63.6 5.8±0.3; 5.4–6.0 34±0.4; 33.6–34.5 62.8±2.2; 60–64.6 13.0±0.4; 12.1–13.8 22.1±0.7; 21.0–23.2 22.1±0.8; 20.8–24.7 12.7±0.8; 11.6–14.2 20.6±0.7; 19.5–21.8 20.9±0.6; 19.7–21.9 15.4±0.7; 13.6–16.5 15.5±0.5; 14.9–16.2 16.1±0.7; 14.9–17.3 45.0±1.9; 43.1–48.1 43.4±1.3; 41.0–45.7 43.7±1.4; 39.9–45.9 40.9±1.0; 39.4–42.7 38.6±1.6; 35.1–39.6 65.6±3.1; 62.3–70.6 TABLE 1 TABLE 42 57.4 52.7 44.4 104.7 141.7 (n=11) Culmen 42.8; 45.9 147; 148; 157 31.1±1.1; 29.3–33.3 51.8±1.5; 47.5–53.8 52.0±1.5; 47.4–55.5 12.2±0.5; 11.6–12.9 30.1±0.7; 29.2–31.2 50.0±1.3; 48.4–51.7 49.0±1.8; 46.0–53.9 46.5±2.0; 41.2–50.1 41.8±1.8; 39.1–43.7 47.7±1.8; 44.5–51.3 82.9±1.1; 81.8–84.4 161.8±4.6; 157–167 95.5±3.3; 92.1–99.8 169.6±1.7; 168–172 118.7±4.0; 111.9–128 116.6±3.7; 108.3–124 117.2±5.6; 109.6–125.7 113.6±2.0; 110.7–117.5 9 8 1 1 6 4 1 4 7 2 1 1 1 5 3 22 20 46 10 18 38 29 21 27 12 (n) 1,1,2 Birds Sample F F F F F F F F F F F F M M M M M M M M M M M M M Sex M,F,? Measurements Measurements of wintering albatrosses and petrels of Brazil sampled at sea in 2006 and 2007 Macronectes halli Macronectes Puffinus griseus Puffinus Puffinus gravis Puffinus Daption capense Diomedea exulans Oceanites oceanicus Diomedea dabbenena Calonectris diomedea Fulmarus glacialoides Macronectes giganteus Macronectes White-chinned Petrel aequinoctialis Procellaria Spectacled Petrel conspicillata Procellaria Cory’s Shearwater Cory’s Great Shearwater Wilson’s Storm-Petrel Wilson’s Black-browed Albatross Black-browed melanophris Thalassarche Albatross Yellow-nosed Atlantic chlororhynchos Thalassarche Northern

Wandering Albatross Wandering Tristan Albatross Tristan

Some measurements could not be taken because of moult. Sample size appears in parentheses. For For sample sizes up to 3, raw values are in given, by individual bird; otherwise, values are as given mean and range. Procellariidae: Procellariinae Hydrobatidae Procellariidae: Fulmariinae a b Species Diomedeidae

Marine Ornithology 37: 253–260 (2009) 256 Bugoni & Furness: Age composition and sexual size dimorphism of albatrosses and petrels

Age composition of the community Sexual size dimorphism

The community of in the southwest Atlantic Males were larger than females in all species studied, although there was composed mostly of juveniles of some species such as Black- was considerable overlap between the sexes in linear measurements browed Albatross, Southern Giant Petrel Macronectes giganteus (Table 1). The SSD was more conspicuous for Southern Giant and probably Cape Petrel Daption capense and Southern Fulmar Petrel, with females being 82% the size of males, and for Fulmarus glacialoides; but, for other species, such as White-chinned Wandering Albatross (Table 3). The SSD was less pronounced or Petrel Procellaria aequinoctialis, Great Shearwater Puffinus gravis absent for some traits in Great Shearwater. and Atlantic Yellow-nosed Albatross, a mix of immatures and adults was found (Table 2). For a few species, the adults included Pairs of closely related species—for example, Thalassarche breeders that forage in the region during the breeding period: for albatrosses or Procellaria petrels—did not show consistent SSD example, Atlantic Yellow-nosed Albatross (as indicated by moult (Table 3). The SSD was more accentuated for Atlantic Yellow- condition and the presence of a brood patch) and Wandering nosed Albatross than for Black-browed Albatross and for Spectacled Albatross with rings identifying them as individuals known from Petrel Procellaria conspicillata than for White-chinned Petrel. studies at the breeding colony to have chicks at the time of their capture off Brazil. Morphometric differences in sister species and in relation to age

Atlantic Yellow-nosed Albatross males and females are generally TABLE 2 smaller than Black-browed Albatross (Table 1). For males, Age classes of albatrosses and petrels sampled at sea significant differences after Bonferroni correction were detected in 2006 and 2007 in the Southwestern Atlantic only for wing length (Mann–Whitney U = 3.6, P = 0.0003); for Species First Immature Adults Birds females, significantly different traits were culmen (U = 2.6, P = year sampled 0.09), bill height (U = 4.1, P < 0.0001), tarsus (U = 4.5, P < (n) 0.0001) and wing (U = 3.9, P < 0.0001). Tail length was greater but Tristan Albatross 0 1 3 4 nonsignificant in female Atlantic Yellow-nosed Albatrosses (U = Diomedea dabbenena 1.8, P = 0.07). However, measurements overlapped greatly, and species separation based solely on measurements is not feasible. Wandering Albatross 1 0 8 9 Diomedea exulans The Spectacled Petrel was slightly smaller than the White-chinned Black-browed 25 6 2 33 Petrel for all parameters (Table 1) except for bill depth, but for Albatross Thalassarche males and females alike, values were not significantly different for melanophris most morphometric measurements (culmen, bill depth, tarsus) after Bonferroni correction (P < 0.01). The only significant differences Atlantic Yellow-nosed 0 16 17 33 were for non-skeletal traits—that is, wing (U = 23.5, P < 0.0001 for Albatross Thalassarche males; U = 1.5, P = 0.003 for females) and tail length (U = 5.8, P < chlororhynchos 0.0001 for males; U = 3.4, P = 0.0006 for females). In addition, all Southern Giant Petrel 11 0 0 11 distributions of measurements overlapped considerably, precluding Macronectes giganteus separation of individual birds to species even when the sex of the bird was known. Northern Giant Petrel 0 0 1 1 Macronectes halli For Great Shearwater, we tested for differences in size arising with Southern Fulmar 10 0 0 10 age by comparing juveniles with adults. No difference was found for Fulmarus glacialoides tarsus, wing and tail (Mann–Whitney test, all P > 0.05; males and females pooled because SSD was not detected, as described earlier). Cape Petrel Daption 32? 0 0 32 capense DISCUSSION White-chinned Petrel 20? Present Present 30 Procellaria aequinoctialis The range of measurements found in several species was generally greater than published data obtained in breeding grounds, probably Spectacled Petrel 0 Present Present 64 a result of birds from differing origins meeting in the area. That Procellaria conspicillata finding was expected, because species size may vary considerably Cory’s Shearwater 0 1? 1? 2 according to population of origin. For the Southern Giant Petrel, Calonectris diomedea for example, Copello et al. (2006) provided linear measurements Great Shearwater 7 15+ 45? 67 from Argentina and reviewed values from other Antarctic and sub- Puffinus gravis Antarctic locations, and demonstrated that birds from Patagonia, Gough and the Falkland are smaller than those from other Sooty Shearwater 0 1 1 2 populations. Measurements for males and females we captured Puffinus griseus at sea cover the wide range of values of various populations and Wilson’s Storm-Petrel 3 1 0 4 are an indication of the varying origins of sampled birds, in line Oceanites oceanicus with records of banded birds from known locations and diagnostic plumage characteristics (Olmos 2002, Carlos et al. 2005). For ? = age status not confirmed. instance, we sampled one Southern Giant Petrel male significantly

Marine Ornithology 37: 253–260 (2009) Bugoni & Furness: Age composition and sexual size dimorphism of albatrosses and petrels 257 smaller than others, which probably belonged to the M. giganteus In most avian species and families, SSD is male-biased (Székely et solanderi taxon. For other species, multiple origins are possible, al. 2007). In a multispecies analysis, Bull et al. (2005) noted that as demonstrated for Black-browed Albatross (Phillips et al. 2005, Puffinus exhibit low levels of SSD, with some species showing Bugoni & Furness 2009) and for other species (see review in Olmos reversed dimorphism in some traits, as in wing length of Great 2002 of ringed seabirds recovered in Brazil). Shearwater. We found similar values for wing length in both sexes and reversed SSD in tail length, in agreement with Bull et al. Hall (1987) and Ryan (1998) showed that Spectacled Petrel (2005). In general, bill depth was the trait with the larger sexual are smaller than White-chinned Petrel in most morphometric dimorphism towards males in Puffinus (Bull et al. 2005, Haywood measurements (except tarsus and minimum bill depth), which, among & Bull 2008). Our analysis, including more distantly related species other characteristics, warrant it as a biologically valid species (Ryan such as petrels and albatrosses, found that bill depth and culmen 1998). Here, we confirm that male and female Spectacled Petrels length are the measurements with most pronounced dimorphism, are both on average slightly smaller than White-chinned Petrels. also suggesting the bill as the skeletal feature most prone to be However, in our sample of both species captured at sea, interspecific selected for dimorphism in Procellariiformes. differences between linear measurements of skeletal traits (culmen, bill depth at base, tarsus lengths) were not detected. On the other SSD in one trait is often only loosely related to SSD in another trait hand, wing and tail length were highly significantly different, which in Procellariiformes, as demonstrated in a range of other bird taxa, confirm a suggestion of Rowan et al. (1951). These results contrast suggesting that different selective forces are acting on different traits with Ryan (1998) who found differences in 20 Spectacled Petrels (Székely et al. 2007). For several species sampled in this study, birds measured on the breeding grounds at Inaccessible , Tristan da of distinct populations could have been captured, and therefore SSD Cunha group, compared with 72 White-chinned Petrels incidentally could be even more pronounced for some of them. Newton [1979 captured in longline fishery around Prince Edward Island, Indian (in Hunter 1987)] showed that there is a relationship between the Ocean. He found differences for culmen, bill depth at base, bill type of prey taken and the magnitude of SSD. For Giant Petrels, depth at nail, wing and mass, but not in bill minimum depth and it is suggested that the marked sexual dimorphism in all variables tarsus. Morphometric differences, segregation in breeding islands, including bill is related to feeding strategies, with males relying more differences in vocalizations and different breeding periods were on terrestrial food (carrion) and females, on marine food (Hunter 1987, used to assure full specific status for the Spectacled Petrel (Ryan González-Solís et al. 2008). Sexual segregation in foraging areas has 1998). Results of measurements presented here from a pool of birds been demonstrated for some species with more marked dimorphism at sea, and controlling for sex, were slightly different; but based on in size (e.g. Shaffer et al. 2001, González-Solís et al. 2008) and other evidence provided by Ryan (1998) and clear segregation at could explain the skewed sex ratios based on SSD in several species sea between Spectacled and White-chinned petrels (Neves et al. (Table 3), in which niche segregation by diving or feeding tactics is 2006) and derived from satellite-tracked birds (Bugoni et al. 2009), more difficult to demonstrate for sympatric males and females at sea. they confirm the distinctiveness of these taxa. Our results suggested For other species, it is less clear how and why sexual dimorphism that comparisons based solely on adults or measurements from evolved, but males are larger in all Procellariiformes studied here, specific colonies could differ from comparisons of birds of different and more pronounced bill traits suggest that territorial defence of the populations and age classes sampled at sea, as probably occurred nest could play a role (Bull et al. 2005). However, that hypothesis is with the Procellaria petrels that we sampled. hard to distinguish from sexual selection, which is also a plausible TABLE 3 Sexual size dimorphism (female:male ratio) in external body measurements of albatrosses and petrels sampled at sea off Brazil, based on samples reported in Table 1 Species Culmen Bill depth Tarsus Wing Tail Wandering Albatross Diomedea exulans 0.82 0.96 0.93 0.94 1.00 (P<0.05) (P<0.05) (P<0.05) Black-browed Albatross Thalassarche melanophris 0.99 0.97 0.97 0.97 0.93 (P<0.01) (P<0.05) Atlantic Yellow-nosed Albatross Thalassarche chlororhynchos 0.96 0.94 0.95 0.98 0.97 (P<0.001) (P<0.001) (P<0.001) (P<0.05) Southern Giant Petrel Macronectes giganteus 0.87 0.88 0.89 0.92 0.95 (P<0.01) (P<0.01) (P<0.05) (P<0.01) Southern Fulmar Fulmarus glacialoides 0.94 0.92 0.93 0.95 0.94 Cape Petrel Daption capense 0.97 0.98 0.96 0.98 0.98 (P<0.05) (P<0.05) White-chinned Petrel Procellaria aequinoctialis 0.97 0.93 0.99 0.99 0.99 (P<0.001) (P<0.001) Spectacled Petrel Procellaria conspicillata 0.94 0.95 0.97 0.97 0.99 (P<0.001) (P<0.001) (P<0.001) (P<0.01) Great Shearwater Puffinus gravis 0.97 0.96 0.99 1.00 1.02 (P<0.01)

Marine Ornithology 37: 253–260 (2009) 258 Bugoni & Furness: Age composition and sexual size dimorphism of albatrosses and petrels explanation. Preferences for access to discards from fishing vessels Atlantic, and Macaronesian Islands in the North Atlantic. Variation and to food of a given size has been demonstrated between seabird in age composition throughout the year could not be addressed here, species according to body size (Furness et al. 1988, Ballance 2007 but deserves further study, particularly for species of conservation and references therein). Food resource partitioning could also vary concern and known to be incidentally captured in fisheries throughout between the sexes in species with marked SSD. the year in the area (Neves et al. 2007; Bugoni et al. 2008a, 2008c).

Fairbairn & Shine (2003) found that larger seabird species tended ACKNOWLEDGEMENTS to show larger differences in SSD, in their case measured as body mass. Despite problems associated with their analysis [body mass Thanks are due to Captain Celso Oliveira and crew of the fishing is very variable (see Croxall 1995, Shine & Fairbairn 1995)], we vessels Ana Amaral I and Akira V for logistics support onboard. found—when using linear single-dimensional measurements— Thanks are also due to Kate Griffiths for lab work on molecular the same pattern for albatrosses (Diomedeidae) and petrels and sexing of birds and to Richard Griffiths for providing us the shearwaters (Procellariidae). Weidinger & van Franeker (1998) primer 2757R. LB received a CAPES Scholarship. This study was mention that the Cape Petrel is one of the least dimorphic among carried out according to permits No. 0128931BR, No. 203/2006, fulmarines, in agreement with our data (Table 3). However, SSD No. 02001.005981/2005, No. 023/2006, No. 040/2006 and is of the same magnitude or even less conspicuous in some other No. 1282/1, all granted by the Brazilian Environmental Agency Procellariiformes studied here, such as White-chinned Petrel, Great (IBAMA), and to International Health Certificate No. 0975- Shearwater and Black-browed Albatross. 06, issued by the Brazilian Government. The Scottish Executive– Rural Affairs Directorate also kindly provided the permit POAO Based on linear measurements alone, we also failed to distinguish 2007/91 to import samples into Scotland. sister Procellaria and Thalassarche species despite significant differences in some traits. The degree of overlap is high even when REFERENCES the sex is known, and it precludes species identification of partial carcasses frequently found stranded on beaches. Future studies AYRES, M., AYRES, M. Jr, AYRES, D.L. & SANTOS, A.A.S. using discriminant function analysis could be more successful in 2007. BioEstat v.5, aplicações estatísticas nas áreas das ciências separating these closely related species. biomédicas. Belém, Brazil: Sociedade Civil Mamirauá, MCT- CNPq. Age composition of the pelagic community BALLANCE, L.T. 2007. Understanding seabirds at sea: why and how? Marine Ornithology 35: 127–135. For some species, such as Black-browed Albatross, White-chinned BARBRAUD, C. & CHASTEL, O. 1998. Southern Fulmars molt Petrel and Southern Giant Petrel, most individuals in the area were their primary feathers while incubating. Condor 100: 563–566. juveniles. For others, juveniles, immatures, breeding or non-breeding BECK, J.R. 1969. Food, moult and age of first breeding in the Cape adults shared the area, even during the breeding period. Particularly Pigeon, Daption capensis Linnaeus. British Antarctic Survey remarkable was the presence of a large number of breeding adult Bulletin 21: 33–44. Atlantic Yellow-nosed Albatrosses, which breed only in the Tristan BRIDGE, E.S. 2006. Influences of morphology and behavior on da Cunha Islands. It is not clear if breeding Spectacled Petrels, which wing-molt strategies in seabirds. Marine Ornithology 34: 7–19. also nest on Islands, also forage in Brazilian waters BUGONI, L. 2006. Great-winged Petrel Pterodroma macroptera in during their breeding period. However, all birds of that species we Brazil. Bulletin of the British Ornithologists’ Club 126: 52–54. captured during the breeding period were immatures or adults, with BUGONI, L. & FURNESS, R.W. 2009. Ageing immature Atlantic no juveniles, which is surprisingly and suggests that juveniles occur Yellow-nosed Thalassarche chlororhynchos and Black-browed in a different area. Furthermore, because juveniles are generally more T. melanophris albatrosses in wintering grounds using bill prone to be killed in fisheries, the absence of juvenile Spectacled colour and moult. Marine Ornithology 37: 249–252. Petrels in the area could explain why this abundant species attending BUGONI, L., NEVES, T.S., ADORNES, A.C., OLMOS, F. & longline vessels has low capture rates in comparison with the BARQUETE, V. 2003. Northern Giant Petrel Macronectes halli similar White-chinned Petrel (Bugoni et al. 2008c). Great Shearwater in Brazil. Atlantic Seabirds 5: 127–129. juveniles and immatures occured in the area during the breeding BUGONI, L., NEVES, T.S., LEITE, N.O. Jr, CARVALHO, D., period, with the latter carrying out extensive moult in Brazilian waters. SALES, G., FURNESS, R.W., STEIN, C.E., PEPPES, F.V., Species from the Antarctic, such as Cape Petrel and Southern Fulmar, GIFFONI, B.B. & MONTEIRO, D.S. 2008a. Potential bycatch occur in the area exclusively during winter–spring and are probably of seabirds and turtles in hook-and-line fisheries of the Itaipava composed mostly of juveniles, but the rapid moult undertaken by these Fleet, Brazil. Fisheries Research 90: 217–224. species (Beck 1969, Barbraud & Chastel 1998) precludes accurate BUGONI, L., NEVES, T.S., PEPPES, F.V. & FURNESS, R.W. age determination of birds captured in mid-winter. For Wandering 2008b. An effective method for trapping scavenging seabirds at Albatross, we captured ringed male and female birds rearing chicks on sea. Journal of Field Ornithology 79: 308–313. South Georgia Island, and also juveniles and birds in sabbatical year, BUGONI, L., MANCINI, P.L., MONTEIRO, D.S., NASCIMENTO, demonstrating the importance of the area for all age classes and sexes. L. & NEVES, T.S. 2008c. Seabird bycatch in the Brazilian That finding is probably true for Tristan’s Albatross, because juveniles pelagic longline fishery and a review of capture rates in the and adults were captured; however, none had previously been ringed. southwestern . Endangered Species Research 5: 137–147. Overall, the pelagic community of seabirds off the Brazilian coast is BUGONI, L., D’ALBA, L. & FURNESS, R.W. 2009. Marine habitat composed of birds of various ages and breeding status according to use of wintering Spectacled Petrels Procellaria conspicillata, species. Birds originate from a wide range of breeding areas, including and overlap with longline fishery. Marine Ecology Progress Tristan da Cunha, Falklands and South Georgia Islands in the South Series 374: 273–285.

Marine Ornithology 37: 253–260 (2009) Bugoni & Furness: Age composition and sexual size dimorphism of albatrosses and petrels 259

BULL, L.S., BELL, B.D. & PLEDGER, S. 2005. Patterns of size MARTUSCELLI, P., SILVA-E-SILVA, R. & OLMOS, F. 1997. variation in the Shearwater Genus Puffinus. Marine Ornithology A large Prion Pachyptila wreck in south-east Brazil. Cotinga 33: 27–39. 8: 55–57. CARLOS, C.J., VOISIN, J.F. & VOOREN, C.M. 2005. Records MAYER, F.P. & ANDRADE, H.A. 2005. Swordfish (Xiphias of Southern Giant Petrel Macronectes giganteus solanderi and gladius) and Blue Shark (Prionace glauca) fishery and the Northern Giant Petrel M. halli off southern Brazil. Bulletin of dynamics of the fleet off the southeastern Brazilian coast. the British Ornithologists’ Club 125: 288–292. Collective Volumes of Scientific Paper, ICCAT 58: 1204–1214. CATRY, P., PHILLIPS, R.A. & FURNESS, R.W. 1999. Evolution NEVES, T. & OLMOS, F. 1997. Albatross mortality in fisheries of reversed sexual size dimorphism in skuas and jaegers. Auk off the coast of Brazil. In: Robertson, G. & Gales, R. (Eds). 116: 158–168. Albatross, biology and conservation. Chipping Norton, UK: CBRO (COMITÊ BRASILEIRO DE REGISTROS Surrey Beatty and Sons. pp. 214–219. ORNITOLÓGICOS). 2009. Lista das aves do Brasil. Eighth NEVES, T., VOOREN, C.M., BUGONI, L., OLMOS, F. & ed. 9 August 2009. São Paulo, Brazil: Comitê Brasileiro de NASCIMENTO, L. 2006. Distribuição e abundância de aves Registros Ornitológicos, Sociedade Brasileira de Ornitologia. marinhas no sudeste-sul do Brasil. In: Neves, T., Bugoni, L. [Available online at: http://www.cbro.org.br/CBRO/listapri. & Rossi-Wongtschowski, C.L.B. (Eds). Aves oceânicas e suas htm; accessed August 2009] interações com a pesca na região Sudeste-Sul do Brasil. São COPELLO, S., QUINTANA, F. & SOMOZA, G. 2006. Sex Paulo, Brazil: USP-REVIZEE. pp. 11–35. determination and sexual size-dimorphism in Southern Giant- NEVES, T., MANCINI, P.L., NASCIMENTO, L., MIGUÉIS, Petrels (Macronectes giganteus) from Patagonia, Argentina. A.M.B. & BUGONI, L. 2007. Overview of seabird bycatch Emu 106: 141–146. by Brazilian fisheries in the South Atlantic Ocean. Collective CROXALL, J.P. 1995. Sexual size dimorphism in seabirds. Oikos Volumes of Scientific Papers, ICCAT 60: 2085–2093. 73: 399–403. OLMOS, F. 1997. Seabirds attending bottom long-line fishing off CUTHBERT, R.J., PHILLIPS, R.A. & RYAN, P.G. 2003. Southeastern Brazil. Ibis 139: 685–691. Separating the Tristan Albatross and the Wandering Albatross OLMOS, F. 2002. Non-breeding seabirds in Brazil: a review of using morphometric measurements. Waterbirds 26: 338–344. band recoveries. Ararajuba 10: 31–42. FAIRBAIRN, J. & SHINE, R. 1993. Patterns of sexual size OLMOS, F. & BUGONI, L. 2006. Agregações de aves marinhas dimorphism in seabirds of the . Oikos 68: associadas à pesca de espinhel-de-fundo na região Sudeste-Sul 139–145. do Brasil. In: Neves, T., Bugoni, L. & Rossi-Wongtschowski, FOWLER, J., COHEN, L. & JARVIS, P. 1998. Practical statistics C.L.B. (Eds). Aves oceânicas e suas interações com a pesca for field biology. Second edition. Chichester, UK: John Wiley na região Sudeste-Sul do Brasil. São Paulo, Brazil: USP- and Sons. 259 pp. REVIZEE. pp. 69–81. FRIDOLFSSON, A.K. & ELLEGREN, H. 1999. A simple and OLMOS, F., MARTUSCELLI, P., SILVA, R.S. & NEVES, T.S. universal method for molecular sexing of non-ratite birds. 1995. The seabirds of São Paulo, southeastern Brazil. Bulletin Journal of Avian Biology 30: 116–121. of the British Ornithologists’ Club 115: 117–128. FURNESS, R.W., HUDSON, A.V. & ENSOR, K. 1988. Interactions OLMOS, F., NEVES, T.S. & BASTOS, G.C. 2001. A pesca between scavenging seabirds and commercial fisheries around com espinhéis e a mortalidade de aves marinhas no Brasil. In: the British Isles. In: Burger, J. (Ed). Seabirds and other marine Albuquerque, J.L.B., Cândido, J.F. Jr, Straube, F.C. & Roos, vertebrates: competition, predation, and other interactions. New A.L. (Eds). Ornitologia e conservação, da ciência às estratégias. York, USA: Columbia University Press. pp. 240–268. Tubarão, Brazil: Editora Unisul. pp. 327–337. GARCIA, C.A.E. 1998. Oceanografia física. In: Seeliger, U., ONLEY, D. & SCOFIELD, P. 2007. Albatrosses, petrels and Odebrecht, C. & Castello, J.P. (Eds). Os ecossistemas costeiro shearwaters of the world. Princeton, USA: Princeton University e marinho do extremo sul do Brasil. Rio Grande, Brazil: Press. 240 pp. Ecoscientia. pp. 104–106. PHILLIPS, R.A., SILK, J.R.D., CROXALL, J.P., AFANASYEV, GONZÁLEZ-SOLÍS, J., CROXALL, J.P. & AFANASYEV, V. V. & BENNETT, V.J. 2005. Summer distribution and migration 2008. Offshore spatial segregation in Giant Petrels Macronectes of nonbreeding albatrosses: individual consistencies and spp.: differences between species, sexes and seasons. Aquatic implications for conservation. Ecology 86: 2386–2396. Conservation: Marine and Freshwater Ecosystems 17: S22–S36. PRINCE, P.A. & RODWELL, S.P. 1994. Ageing immature Black- HALL, A.J. 1987. The breeding biology of the White-chinned browed and Grey-headed Albatrosses using moult, bill and Petrel Procellaria aequinoctialis at South Georgia. Journal of plumage characteristics. Emu 94: 246–254. Zoology (London) 212: 605–617. ROWAN, A.N., ELLIOT, H.F.I. & ROWAN, M.K. 1951. The HAYWOOD, J. & BULL, L.S. 2008. Allometry and phenotypic “Spectacled” form of the Shoemaker Procellaria aequinoctialis variation in the morphometrics of Puffinus shearwaters. Marine in the Tristan da Cunha Group. Ibis 93: 169–179. Ornithology 36: 53–57. RYAN, P.G. 1998. The taxonomic and conservation status of the HUNTER, S. 1987. Species and sexual segregation mechanisms in Spectacled Petrel Procellaria conspicillata. Bird Conservation sibling species of Giant Petrels Macronectes. Polar Biology 7: International 8: 223–235. 295–301. SHAFFER, S.A., WEIMERSKIRCH, H. & COSTA, D.P. 2001. LIMA, P.C., GRANTSAU, R., LIMA, R.C.F.R. & SANTOS, S.S. Functional significance of sexual dimorphism in Wandering 2004. Occurrence and mortality of seabirds along the northern Albatrosses, Diomedea exulans. Functional Ecology 15: 203– coast of Bahia, and the identification key of the Procellariiformes 210. order and the Stercorariidae family. Atualidades Ornitológicas SHINE, R. & FAIRBAIRN, J. 1995. Sexual size dimorphism in 121: 1–63. seabirds: a reply to Croxall. Oikos 74: 146–148.

Marine Ornithology 37: 253–260 (2009) 260 Bugoni & Furness: Age composition and sexual size dimorphism of albatrosses and petrels

SICK, H. 1997. Ornitologia Brasileira. Rio de Janeiro, Brazil: Nova WEIDINGER, K. & VAN FRANEKER, J.A. 1998. Applicability Fronteira. 912 pp. of external measurements to sexing of the Cape Petrel Daption SZÉKELY, T., LISLEVAND, T. & FIGUEROLA, J. 2007. Sexual capense at within-population and between-population scales. size dimorphism in birds. In: Blanckenhorn, W., Fairbairn, D. Journal of Zoology (London) 245: 473–482. & Székely, T. (Eds). Sex, size and gender roles. Oxford, UK: Oxford University Press. pp. 27–37.

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