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Volume 2014 (2014), Article ID 907549, 16 pages
Reproductive Dynamics of Sterna hirundinacea Lesson, 1831 in Ilha dos Cardos, Santa Catarina, Brazil
1Universidade Federal de São Carlos, CP 676, 13565-905 São Carlos, SP, Brazil
2Centro de Ensino em Ciências Tecnológicas da Terra e do Mar, UNIVALI, CP 360, 88301-970, Itajaí, SC, Brazil
3Setor de Biodiversidade e Ecologia, Instituto de Ciências Biológicas e da Saúde, Universidade Federal de Alagoas, Praça Afranio Jorge, s/n, Prado, 57010-020 Maceió, AL, Brazil
4Azorean Biodiversity Group (CITA-A) and Platform for Enhancing Ecological Research & Sustainability (PEERS), Departamento de Ciências Agrárias, Universidade dos Açores, Rua Capitão João D’Ávila, 9700-042 Angra do Heroísmo, Portugal
Received 20 January 2014; Accepted 8 May 2014; Published 28 May 2014
Academic Editor: Pablo M. Vergara
Copyright © 2014 Hélio Augusto Alves Fracasso et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
In this work, we intend to describe the reproductive dynamics of Sterna hirundinacea in an island from South Brazil. We studied the reproductive biology of this species in its natural environment and provide data on their growth, survival, and reproductive success in Ilha dos Cardos, Santa Catarina, South Brazil. Samplings were carried out daily on the island throughout the reproductive seasons of 2003, 2005, and 2006 and the different stages of development of the chicks were characterized according to age, length of the beak, and plumage characteristics. We provide a basic equation to determine the approximate age of individuals using their body mass. The main cause of chick mortality on the island was natural (63.17% in 2003, 81.41% in 2005, and 79.96% in 2006), whereas predation contributed to mortality in a proportion of 38.83% in 2003, 18.59% in 2005, and 20.04% in 2006. The absence in the area of the chicks’ main predator, Kelp gull (Larus dominicanus), the large number of chicks that reached the final stages of development, and their reproductive success demonstrate that Ilha dos Cardos is an important breeding site for the species in southern Brazil.
The South American Tern, Sterna hirundinacea Lesson, 1831, is distributed in the Atlantic coast of South America, from southeastern Brazil to Tierra del Fuego in Argentina/Chile, including the Falkland Islands and the Pacific coast to southern Peru [1, 2], with one record for riverine environments in Rio Negro, Argentina .
The species is almost exclusively coastal, nesting on sandy or rocky beaches, cliffs, and small islands . In the Brazilian coasts, nests are found in coastal islands from Santa Catarina [5, 6] to Espírito Santo , from April to August, usually in sympatry with Cabot’s Tern, Thalasseus acuflavidus (Cabot, 1847) [6, 8, 9]. The South American Tern nests singly in scattered nests; their eggs and chicks are dark and effectively do mimics of their surroundings . Chicks abandon the nests after their first week of life and seek shelter beneath neighboring vegetation [6, 8, 11].
Patterns of growth in birds are a result of evolutionary adaptations to environmental factors [12, 13] and were first qualitatively studied by describing the developmental stages in a series, followed by quantitative formulations that consider growth as a result of a network of simultaneous metabolic processes . According to Nisbet et al. , differences in the growth patterns of chicks have been used to explore parental performance variations, whereas differences in mean parameters of colony growth over the years have been used to explore differences in average environmental conditions. It is known that the postnatal development of seabirds can be a sensitive indicator of local environmental conditions [16, 17] and has been evaluated for many species [18–21].
The breeding biology of South American Terns was described by Fracasso et al. , their reproductive success by Fracasso and Branco , and the foraging comparison with Cabot’s Terns by Fracasso et al. . In this study, we investigated the reproductive biology of the South American Tern in its natural environment, with the objective of giving information on growth, survival, and reproductive success of a population breeding in Cardos Island following the pioneering work of Branco . Furthermore, we provide a hypothesis that, with the basic equation formed by these three-year data, we will determine the approximate age of individuals using their mass, providing more tools for the species conservation, since management of endangered bird species does require an accurate knowledge of specific breeding events such as hatching dates and growth of chicks .
Sampling was carried out daily at Ilha dos Cardos (27°48′55′′ S, 48°34′52′′ W), Florianópolis, Santa Catarina (Figure 1), during the breeding seasons of 2003, 2005, and 2006.
According to the incidence of coupling and nests, seasons were divided into three periods: early (12/05 to 04/07), medium (05/07 to 11/08), and late (from 12/08). The chicks were sampled by direct counting according to their age. The number of dead chicks was obtained from rigorous searches conducted periodically throughout the island, when dead bodies were collected and counted. All dead chicks (regardless of the cause of death: lack of food, drowning, and territorial fights or being preyed on by hawks and vultures) were collected and disposed of to avoid counting them more than once. We followed a nest in the center of the colony, which had two eggs, daily during the 2006 season; the chicks were photographed and key changes in their plumage were recorded (Figure 16).
In order to monitor chicks daily, we installed individual enclosures (1 m2) (Figure 2) around each new posture, using fishing lines, iron hooks, and gill nets (mesh 1.0 cm), in an adaptation of the method described by Efe et al. .
We did this to prevent the chicks from running away and getting lost in the vicinity of the nest [23, 25]. The chicks inside and outside the enclosures were tagged and followed (Table 1) in order to conduct comparisons and analyze possible changes in growth caused by the stress of daily recapture.
Juveniles and adults were captured using mist nets as described in CEMAVE-IBAMA . In this study, the measurements of the culmen (Lt beak) and tarsus (Lt tarsus) are presented in order to characterize the pattern of linear dimension of the body in the study population, and growth was mostly calculated based on the mass of the chicks. The biometrics of the culmen (Lt beak) and the length in centimeters of the tarsus (Lt tarsus) were taken using a caliper of 0.05 mm and the weight, expressed in grams (Wt), was measured using a 60, 100, 300, and 500 g PESOLA, with a precision of, respectively, 1, 2, 3, and 5 g .
2.2. Data Processing and Analyses
The Von Bertalanffy model was adjusted and adapted to the growth of juvenile terns, using the body mass, according to the formula , where Lm is the weight in grams, is the maximum mass of juveniles, is the constant of growth, is the time in days, and is the age at birth.
Measurements of the chicks’ body structures registered in the 2003, 2005, and 2006 breeding seasons were analyzed using ANOVA, which tested for homogeneity of variance (Bartlett’s test) and normal distribution (Kolmogorov-Smirnov test) . When significant differences were found, the contrast of means (Tukey-Kramer) was applied to indicate which were significantly different.
3.1. Age Characterization
The different stages of development of the chicks were established according to their age, length of the beak culmen (Figure 10), and plumage characteristics. Thus, Juvenile I (JI) corresponded to the hatchlings usually found in the nest, with the “egg tooth” (structure at the nozzle tip used to break the egg from the inside) (Figure 3) and Ltbeak average cm between 1 and 6 days, with yellow-cream plumage throughout the body (Figure 3).
Juvenile II (JII) corresponded to individuals without the “egg tooth” (Figure 4), tarsus thick enough for the final metal tag, 7 to 14 days old, Ltbeak average , with white breast and yellow-cream plumage on the rest of the body (Figure 4).
Juvenile IV (JIV) corresponded to chicks with well-developed retrix feathers, Ltbeak mean , without yellow-cream plumage, and aggressive behavior, 29 to 37 days old (Figure 6).
Juveniles (Jv) had mean Ltbeak cm, were 38 days old or older, had no trace of the chick plumage, and were already able to fly (Figure 7).
3.2. Age Group Distribution
In 2003, the first eggs hatched in July, with a large increase in the numbers of JI until mid-July (15/07, ), followed by a sharp fall; this trend in fluctuating daily abundance was recorded for all subsequent ages, with the greatest numbers of JII in late July (26/07, ), JIII in early August (03/08, ), and JIV in mid-August (12/08, ); the young began to emerge in late July (29/07), about 38 days after the first outbreaks, with the greatest abundance in late August (24/08, ) and a gradual decrease until the abandonment of the colony.
In 2005, there were three outbreak peaks, the first and largest at the end of June (21/06, ), the second in early August (11/08, ), and the last, and smallest, in mid-September (14/09, ). The peak abundance of other ages was observed in early July (JII: 05/07, and JIII: 10/07, ) and late July (JIV: 22/07, and Jv: 31/07, ), respectively.
In 2006, the first chick was recorded in late May (31/05), with a gradual increase of JI until the end of June (20/06, ), followed by a steady decrease in their numbers until the absence of neonates at the end of the reproductive period. Still early in the season, in mid-June, the numbers of JII were the greatest (29/06, ), whereas peaks in the numbers of JIII (09/07, ) and JIV (17/07, ) occurred in mid-July. According to the same figure, the number of individuals in the juvenile phase fluctuated from the end of July (24/07, ) to mid-August (19/08, ), with gradual abandonment of the colony by the end of September.
3.3. Chicks’ Mortality
The main cause of chicks’ mortality at Cardos Island was natural, accounting for 63.17% of deaths in 2003, 81.41% in 2005, and 79.96% in 2006, whereas predation contributed to 38.83%, 18.59%, and 20.04%, respectively (Figure 8).
In 2003, mortality from natural causes affected mainly young JI and JII in the middle of the reproductive period; predation, on the other hand, was more intense when chicks reached JIII, from the middle to the end of the breeding season. In 2005, natural causes were more prevalent at the beginning of the season, killing JIs and JIIs, and in the middle and end of it, killing JIIIs. Predation, by contrast, was the main mortality factor for JIVs and Jvs at the end of the breeding season. In 2006, mortality from natural causes was a result of fights for territory early in the season (on younger chicks) and lack of food at the end (JIII, JIV, and Jv), along with predation of older individuals in the middle of the reproductive period.
During the breeding seasons, an increase in the size of the beak was observed throughout the development, but these did not reach the adult size while individuals stayed in the colony. There were no differences in the size of the beak of chicks up to 23 days in the three years of study. However, in 2006, growth rates were higher and chicks remained on site for a fewer number of days (Figure 9).
Mean beak measurements were the following for each developmental state, as defined in this work: JI cm, JII , JII , JIV , Jv , and adults cm.
The ANOVA test did not detect significant differences in beak measurements during the study for age groups JII ( = 0.72; ) and JIII ( = 2.53; ). Significantly higher values, by contrast, were found for JI ( = 7.69; ), JIV ( = 6.56; ), Jv ( = 57.11; ), and adults ( = 6.77; ) in 2006.
The greatest daily increase in structure size was observed for the tarsus until day 17; after that, tarsal length increased slowly up to day 38 (Figure 11).
The highest growth rate for this structure was then observed from age group JI ( cm) to JII ( cm), with small increases in JIII ( cm) and JIV ( cm). The tarsus of juveniles resembled ( cm) the means observed for the adults (,02 cm).
According to the results of the ANOVA, significant differences in the size of the tarsus were observed at all ages, with the greatest values found in 2006, the year responsible for most variation in JI ( = 30.82; ), JIII ( = 92.69; ), JIV ( = 156.10; ), Jv ( = 4.98; ), and adults ( = 7.36; ). The smallest variation was observed in 2005 for JII ( = 7.91; ) (Figure 12).
The daily gain in mass from the first to the 20th day of life was considerable for S. hirundinacea chicks at Ilha dos Cardos (19.00 to 115.00 g), with a small increase in the curve until day 37 (143.42 g), when the chicks started to take short flights at the edge of the colony, thereby losing some weight (Figure 13).
In all three stages, chick development was high, from g to JII () and JIII ( g), with a small increase for JIV () and a decrease in the Jv phase ( g) and a tendency for the growth curve to stabilize once adulthood was reached ( g) (Figure 14).
Weight varied significantly, according to the ANOVA test, between age groups JI (= 7.35; ) and JIII ( = 18.23; ), reaching the lowest values in 2005, and varied for JII ( = 68.55; ), JIV (= 13.54; ), and adults ( = 9.89; ), particularly in 2003 and 2006, being not significant for Jv ( = 0.35; ).
Chicks in age group JII, which were randomly captured in the colony during 2003, had significantly bigger beaks and more mass than those which remained cloistered; however, the mass of cloistered JIII, JIV, and Jv was greater than of those who remained free at the site (Table 2).
In 2005, we recorded significant differences in beak measurements at age groups JI, JIII, and JIV, caused by the values found for free chicks, whereas the variation in the size of the tarsus was more significant in the younger age group JI and less in groups JIII and JIV. Variation in weight was greater in age groups JI and JIII (Table 2). According to the same table, JI chicks found free in 2006 had significantly larger dimensions in the structures measured than chicks that remained enclosed, with the exception of body mass recorded at age groups JIII, JIV, and Jv.
It took on average days for the chicks to lose their “egg tooth” and to be classified in group JII () (Figure 15). Up to the appearance of feathers on the remiges and rectrices, with consequent classification in age group JIII (), it took on average days. From age group JIII to JIV, characterized by the development of the remiges and rectrices and complete loss of primary feathers on the head, it took longer ( days, ); learning to fly going from age group JIV to Jv took on average days () (Figure 15.)
When the breeding seasons were compared, significant statistical differences were observed in the time required to outgrow age groups JI ( = 16.65; ), JII ( = 28.36; ), and JIII ( = 4.13; ) but not JIV ( = 0.30, ).
The second chick broke at three days after the first; however, it did not survive after the ninth day of nest monitoring, being alive for only six days. The cause of death was malnutrition and competition with its older brother (Figure 16). The first chick grew up alone, reaching the JII stage in six days, JIII in seven days, and JIV in 27 days. After 33 days, with its feathers well developed the chick was able to perform small jumps, temporarily abandoning the fence, and was observed in the nest in the following days, in the presence of its parents (Figure 16).
The Von Bertalanffy growth model for the mass of the young of S. hirundinacea that were surrounded and captured at random, at the Ilha dos Cardos, fit the following equations: in 2003, in 2005, in 2006 (Figure 17), and among the three years.
The fastest rate of growth occurred in the first 20 days of life, with small additions until the flight and the consequent abandonment of the island, approximately on the 46th day in 2003, 45th in 2005, and 42nd in 2006 (Figure 17).
4.1. Age Group Distribution
The postnatal development of seabird chicks can be a sensitive indicator of local environmental conditions [16, 17, 28–30], which makes the use of seabirds to monitor marine environments a feasible practice [29, 30].
Sterna hirundinacea chicks at Ilha dos Cardos, in this study, and in other islands of Santa Catarina, leave the nest after the first two days of life and seek shelter beneath the surrounding vegetation  similar to the description by Nisbet  for S. hirundo (Linnaeus, 1758).
In colonies of S. hirundinacea, the interval between the birth of the first to the second chick was 53.8 hours, and parental care varied between 26 and 29 days , whereas, in Ilha dos Cardos, the time elapsed between the onset of the first to the second chick ranged between 48 and 60 hours, and the parental care interval, from hatching to the chicks’ first flight, was a little longer, approximately 35–41 days, which may be a result of different reproductive phenologies (austral winter for the Brazilian populations and austral summer for the Argentine population) and the various influences of different oceanographic factors (Brazil and Malvinas currents, resp.). Local adaptations influenced directly by the climate affect the availability of seasonal food, and important factors for the growth and development of the offspring import in the cost of foraging , thereby influencing the reproductive success . Also, metabolism increases with the latitude .
4.2. Chicks’ Mortality
In the coast of Espírito Santo, adult S. hirundinacea arise in mid-April and the first chicks begin to emerge in mid-June . In Ilha dos Cardos, chicks were born between 20 and 25 May, and there was a gradual increase in the number of births beginning in June and peaking in September . In the following season (present study), chicks began to emerge in early July with the greatest abundance in August. This variation is considered normal in birds  and has to do with the environmental conditions encountered by the birds in the beginning of the breeding season.
At Ilha dos Cardos, chicks’ mortality is mainly from natural causes. Constant storms during the winter in southern Brazil had been previously recognized as important for other colonies of terns in Brazil [37, 38]. In Argentina, the main causes of death were predation and parental desertion or delays to return to the nest . The absence of L. dominicanus (Lichtenstein, 1823) populations reproducing in Ilha dos Cardos contributed to the low threat of predation, since this predator is the biggest threat to the conservation of terns in Brazil and Argentina [38, 39].
The most critical period in the survival of tern chicks is during the first 10 days of their lives [40–43] and the probability of survival  and the growth curve  of the chicks also show that there is a critical period during the first nine days after the eclosion in the Ilha dos Cardos.
In colonies of the species in Argentina, the chicks’ risk of death decreases, until they acquire a different plumage, between 13 and 17 days of life and from 26 to 28 days of life . The same happens in breeding colonies of T. acuflavidus in Espírito Santo , where the biometric parameters of the studied chicks do not reach the adult size before the preflight period.
4.3. Growth Curve and Chick Ageing
Being a semiprecocious and migratory bird, S. hirundinacea develops rapidly, which is reflected in an accelerated growth rate of the tarsus in the initial stages, when compared with other structures. According to Klaassen , in the species of terns studied by him, the tarsus develops fast and reaches about 90% of its final length midway between birth and recruitment, indicating that all are able to move about. Tarsus and body mass grew more quickly than culmen, attaining asymptotic values at about 14 and 16 days, respectively, for Whiskered Tern Chlidonias hybrid at Lake Grand-Lieu (47°05′ N, 1°39′ W) in western France . This rapid initial growth may be advantageous for allowing the chick to leave the nest within a few days and move from the colony in search of shelter and protection from predators.
According to Branco , S. hirundinacea JI individuals in Ilha Itacolomi and Ilha dos Cardos were not significantly different in terms of average mass, reaching up to 30 g, whereas JIIs from Ilha dos Cardos were significantly heavier. When the chicks reached the JIII stage, however, those from Ilha de Itacolomi were heavier. In this season, according to our data, the mass of the offspring from Ilha dos Cardos followed the same trend until JIII from other years but was larger at JIV and Jv phase.
The relationship between body mass and length of the culmen in S. hirundinacea individuals from Itacolomi and Cardos indicates that the species has negative allometric growth (Wt = 27.5450 Lt1.84908490); consider = 0.8583, with the greatest increases in mass occurring in the initial length classes . The growth curve of Argentina’s population adjusted close to the logistic equation ( = 0.98) .
The growth curves of S. hirundo and S. dougallii (Montagu, 1813) consist of an exponential phase (initial and short), followed by a linear and logarithmic growth, which tends to an asymptotic value at 19 days for the first species and 24 days for the second . The same trend was observed for the growth curve of daily gain in weight of chicks of S. hirundinacea of Ilha dos Cardos, which stabilized later, around the 25th day of life. Nisbet et al. [42, 43] also found that growth predicted chick survival accurately in S. dougallii. In that species, survival could be predicted from body mass growth in the first few days after hatching. In contrast, in T. sandvicensis (Latham, 1787) body mass in the first few days after hatching is not important for survival, suggesting that poor nourishment during an early stage of life could be overcome . Nisbet et al.  suggest that chick growth and survival, which are already manifested during the first days after hatching in Roseate Terns, are primarily determined by parental performance. In Sandwich Terns, it seems relatively easy for most parents to meet the food requirements of their newly hatched chicks .
The probability of survival  and the growth curve  of chicks indicate that there is a critical period during the first nine days after hatching, an aspect also referred to by Hogan et al.  while studying a breeding colony in an islet (Deserta) that is near our own study site. The main causes of death in Argentina were predation (4.8%) and parental desertion or delays to return to the nest (11.1%). The risk of death decreases until the chick acquires another plumage, when it is between 13 and 17 days old . According to the same author, the risk of death increases again when the chicks are between 26 and 28 days of life, and the main causes of death were parental desertion and changes in the frequency of visits to the chicks (8.3%). Hogan et al.  also report predation by L. dominicanus on both eggs and chick as the main cause of reproductive failure in S. hirundinacea. The largest mass was observed in individuals of age groups JIII, JIV, and Jv which remained fenced in. The lower energy expenditure and the absence of displacement around the colony may have been responsible for it. The smallest mass was found in JII individuals that remained cloistered and may have been influenced by use the fence, while suggesting the need to remove it after the critical period of the chicks’ survival. The growth curve equation established in this study can help researchers identify the age of individuals based on their mass. The fact that L. dominicanus does not reproduce in the area, the great amount of chicks reaching adulthood, and the reproductive success demonstrated in the breeding seasons analyzed make Ilha dos Cardos an important breeding site of the species in southern Brazil.
Conflict of Interests
The authors declare that there is no conflict of interests regarding the publication of this paper.
The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Projeto Aves Marinhas for financing this project. The Fundação do Meio Ambiente de Santa Catarina, FATMA, gave them authorization to work at Ilha dos Cardos. They also thank the following students, among others, for their help with field work and triage: Cristiano L. Evangelista, Fernando K. Decker, Juliano C. Hillesheim, and Felipe Freitas Junior. Thanks are due to the anonymous referee that helped improve previous versions of the paper.
- R. Schlatter, “Status and conservation of seabirds in Chile,” in Status and Conservation of the World's Seabirds, P. G. H. Evans, J. P. Croxall, and R. W. Schreiber, Eds., vol. 2, pp. 261–269, ICBP Technical Publication, Cambridge, UK, 1984.
- R. W. Woods, Guide to the Birds of the Falkland Islands, Anthony Nelson, 1988.
- P. F. Petracci, “Diet of sanderling in Buenos Aires province, Argentina,” Waterbirds, vol. 25, no. 3, pp. 366–370, 2002.
- J. del Hoyo, A. Elliott, and J. Sargatal, Handbook of the Birds of the World, vol. 3, Hoatzin to Auks, Lynx Edicions, Barcelona, Spain, 1996.
- J. O. Branco, “Reprodução das aves marinhas nas ilhas costeiras de Santa Catarina, Brasil,” Revista Brasileira de Zoologia, vol. 20, no. 4, pp. 619–623, 2003.
- J. Branco, “Reprodução de Sterna hirundinacea Lesson e Thalasseus sandvicensis Lathan (Aves, Laridae), no litoral de Santa Catarina, Brasil,” Revista Brasileira de Zoologia, vol. 20, no. 4, pp. 655–659, 2003.
- P. T. Z. Antas, “Status and conservation of seabirds breeding in Brazilian waters,” ICBP Technical Publications, vol. 11, pp. 141–158, 1991.
- M. A. Efe, “Aves marinhas das ilhas do Espírito Santo,” in Aves Marinhas Insulares Brasileiras: Bioecologia e Conservação, J. O. Branco, Ed., pp. 101–118, Editora da UNIVALI, Itajaí, Brasil, 2004.
- H. A. A. Fracasso, J. O. Branco, and E. Barbieri, “Reproductive biology of Cabot's Terns on Cardos Island, Santa Catarina, Brazil,” Biota Neotropica, vol. 11, no. 3, pp. 75–81, 2011.
- H. A. A. Fracasso, J. O. Branco, J. Burger, L. F. Silveira, and J. R. Verani, “Breeding biology of South American Tern from Cardos Island, Santa Catarina State, Brazil,” Journal of Oceanography and Marine Sciences, vol. 1, no. 3, pp. 53–64, 2010.
- H. A. A. Fracasso and J. O. Branco, “Reproductive success of South American terns (Sterna hirundinacea) from Cardos Islands, Florianópolis, SC, Brazil,” Anais da Academia Brasileira de Ciencias, vol. 84, no. 2, pp. 527–536, 2012.
- R. E. Ricklefs, “Patterns of growth in birds,” Ibis, vol. 110, no. 4, pp. 419–451, 1968.
- R. E. Ricklefs, “Physiology and Evolution. Review of Murton,” in Avian Breeding Cycles, N. S. Westwood, Ed., Oxford University Press, New York, NY, USA, 1979.
- I. L. Brisbin, C. T. G. Collins Jr., C. White, and D. A. McCallum, “A new paradigm for the analysis and interpretation of growth data: the shape of things to come,” Auk, vol. 104, pp. 552–554, 1987.
- I. C. Nisbet, J. A. Spendelow, and J. S. Hatfield, “Variations in growth of roseate tern chicks,” Condor, vol. 97, no. 2, pp. 335–344, 1995.
- R. E. Ricklefs, “Avian postnatal development,” in Avian Biology, vol. 7, pp. 1–83, Academic Press, New York, NY, USA, 1983.
- P. D. Boersma and J. K. Parrish, “Flexible growth rates in Fork-tailed Storm-Petrels: a response to environmental variability,” Auk, vol. 115, no. 1, pp. 67–75, 1998.
- B. Nelson, Seabirds: Their Biology and Ecology, The Hamlyn Publishing Group Limited, 1980.
- N. P. Langham, “Growth strategies in marine terns,” Studies in Avian Biology, vol. 8, pp. 73–83, 1983.
- J. Warham, The Petrels: Their Ecology and Breeding Systems, Academic Press, London, UK, 1990.
- M. A. Efe, J. L. X. Nascimento, I. L. S. Nascimento, and C. Musso, “Variações Morfológicas e Padrões de Crescimento de Filhotes de Sterna sandvicensis eurygnatha no Brasil,” Biociências, vol. 12, no. 1, pp. 11–19, 2004.
- H. A. A. Fracasso, J. O. Branco, and E. Barbieri, “Comparação do forrageio do trinta-reis-de-bico-vermelho e do trinta-reis-de-bando no Sul do Brasil,” Biota Neotropica, vol. 11, no. 3, 2011, http://www.biotaneotropica.org.br/v11n3/pt/abstract?article+bn03011032011%20ISSN%201676-0603.
- J.-M. Paillisson, F. Latraube, and S. Reeber, “Assessing growth and age of Whiskered Tern Chlidonias hybrida chicks using biometrics,” Ardea, vol. 96, no. 2, pp. 271–277, 2008.
- M. A. Efe, J. L. X. Nascimento, I. L. S. Nascimento, and C. Musso, “Distribuição e ecologia reprodutiva de Sterna sandivicensis eurygnatha no Brasil,” Melopsittacus, vol. 3, no. 3, pp. 110–121, 2000.
- E. W. M. Stienen and A. Brenninkmeijer, “Variation in growth in Sandwich Tern chicks Sterna sandvicensis and the consequences for pre- and post-fledging mortality,” Ibis, vol. 144, no. 4, pp. 567–576, 2002.
- CEMAVE-IBAMA, Manual de Anilhamento de Aves Silvestres, Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Brasília, Brazil, 2nd edition, 1994.
- J. H. Zar, Biostatistical Analysis, Prentice-Hall, New Jersey, NJ, USA, 4th edition, 1999.
- T. T. Fendley and I. L. Brisbin Jr., “Growth curve analyses, a potential measure of the effects of environmental stress upon wildlife populations,” in Proceedings of the 30th International Congress of Game Biologists, vol. 13, pp. 337–350, 1977.
- D. K. Cairns, “Seabirds as indicators of marine food supplies,” Biological Oceanography, vol. 5, no. 4, pp. 261–267, 1987.
- W. A. Montevecchi, “Birds as indicators of change in marine prey stocks,” in Birds As Monitors of Environmental Change, R. W. Furness and J. J. D. Greenwood, Eds., pp. 217–266, Chapman and Hall, London, UK, 1993.
- I. C. T. Nisbet, “Courtship-feeding, egg-size and breeding success in common terns,” Nature, vol. 241, no. 5385, pp. 141–142, 1973.
- J. A. Scolaro, S. Laurenti, and H. Gallelli, “The nesting and breeding biology of the South American tern in Northern Patagonia,” Journal of Field Ornithology, vol. 67, no. 1, pp. 17–24, 1996.
- W. P. Porter, S. Budaraju, W. E. Stewart, and N. Ramankutty, “Calculating climate effects on birds and mammals: impacts on biodiversity, conservation, population parameters, and global community structure,” The American Zoologist, vol. 40, no. 4, pp. 597–630, 2000.
- D. Lack, The Natural Regulation of Animal Number, Claredon Press, Oxford, UK, 1954.
- M. Klaassen, “Growth and energetics of tern chicks from temperate and polar environments,” Auk, vol. 111, no. 3, pp. 525–544, 1994.
- S. Kendeigh, “Parental care and its evolution in birds,” Illinois Biological Monographs, vol. 22, pp. 1–358, 1952.
- F. P. Campos, D. Paludo, P. J. Faria, and P. Martuscelli, “Aves insulares marinhas, residentes e migratórias, do litoral do Estado de São Paulo,” in Aves Marinhas Insulares Brasileiras: Bioecologia e Conservação, J. O. Branco, Ed., pp. 57–82, Editora da UNIVALI, Itajaí, Brasil, 2004.
- M. A. Efe, C. Musso, and L. Glock, “Sucesso Reprodutivo de Thalasseus sandvicensis eurygnathus no Brasil,” Biociências, vol. 13, no. 1, pp. 63–68, 2005.
- P. Yorio and M. A. Efe, “Population status of Royal and Cayenne Terns breeding in Argentina and Brazil,” Waterbirds, vol. 31, pp. 561–570, 2008.
- A. T. Klett and D. H. Johnson, “Variability in nest survival rates and implications to nesting studies,” Auk, vol. 99, no. 1, pp. 77–87, 1982.
- I. C. T. Nisbet, J. Burger, C. Safina, and M. Gochfeld, “Estimating fledging success and productivity in Roseate Terns (Sterna dougallii),” Colon Waterbirds, vol. 13, pp. 85–91, 1990.
- I. C. T. Nisbet, J. A. Spendelow, J. S. Hatfield, J. M. Zingo, and G. A. Gough, “Variations in growth of Roseate Tern chicks: II. Early growth as an index of parental quality,” Condor, vol. 100, no. 2, pp. 305–315, 1998.
- I. C. T. Nisbet, J. S. Hatfield, W. A. Link, and J. A. Spendelow, “Predicting chick survival and productivity of Roseate Terns from data on early growth,” Waterbirds, vol. 22, no. 1, pp. 90–97, 1999.
- A. F. Gross and V. A. Clarck, Survival Distribuitions: Reliability Applications in the Biomedical Sciences, John Wiley and Sons, New York, NY, USA, 1975.
- R. E. Ricklefs, “A graphical method of fitting equations to growth curves,” Ecology, vol. 48, pp. 978–983, 1967.
- J. M. C. Pereira, Comparação da alimentação e crescimento de crias em duas espécies simpátricas de garajau (Sterna hirundo, Sterna dougallii) nos Açores [Tese de Doutoramento], Universidade do Algarve, 1997.
- R. I. Hogan, L. J. Prellvitz, and C. M. Vooren, “Breeding biology of South American tern Sterna hirundinacea (Charadriiformes: Sternidae) on Deserta Island, Southern Brazil,” Revista Brasileira de Ornitologia, vol. 18, no. 3, pp. 207–215, 2010.