Chris P. F. Redfern. 2021: Pair bonds during the annual cycle of a long-distance migrant, the Arctic Tern (Sterna paradisaea). Avian Research, 12(1): 32. DOI: 10.1186/s40657-021-00268-3
Citation:
Chris P. F. Redfern. 2021: Pair bonds during the annual cycle of a long-distance migrant, the Arctic Tern (Sterna paradisaea). Avian Research, 12(1): 32. DOI: 10.1186/s40657-021-00268-3
Chris P. F. Redfern. 2021: Pair bonds during the annual cycle of a long-distance migrant, the Arctic Tern (Sterna paradisaea). Avian Research, 12(1): 32. DOI: 10.1186/s40657-021-00268-3
Citation:
Chris P. F. Redfern. 2021: Pair bonds during the annual cycle of a long-distance migrant, the Arctic Tern (Sterna paradisaea). Avian Research, 12(1): 32. DOI: 10.1186/s40657-021-00268-3
School of Natural & Environmental Sciences, Newcastle University, NE2 4HH & Natural History Society of Northumbria, Great North Museum: Hancock, Newcastle upon Tyne, NE2 4PT, UK
The extent to which pairs remain together during the annual cycle is a key question in the behavioural ecology of migratory birds. While a few species migrate and winter as family units, for most the extent to which breeding partners associate in the non-breeding season is unknown. The Arctic Tern (Sterna paradisaea) has one of the longest migrations of any species, and the aim of this study was to establish whether or not partners remain together after breeding.
Methods
Leg-mounted geolocators were fitted to breeding pairs of Arctic Terns nesting on the Farne Islands, Northumberland, UK. The devices were recovered for analysis the following year.
Results
Analysis of data for the six pairs which returned the following year showed that partners departed from the colony at different times after breeding and migrated independently to different Antarctic regions. Partners also departed from the Antarctic and turned to the breeding colony independently. One third of the pairs divorced on return.
Conclusions
For long-distance migrants reliant on unpredictable foraging opportunities, it may not be viable to remain as pairs away from the breeding colony. Synchrony in arrival times at the breeding colony may maximise the chance of retaining a familiar partner, but could be affected by environmental factors in wintering areas or along migration routes.
Flight is the central avian adaptation and an extraordinary range of specialized modes of flight has been exploited during evolution (Gill 1995). Skeleton and wing muscles form the basis for avian flight; these anatomical features are also adapted to reflect the flight style and phylogeny (McKitrick 1991; Corvidae et al. 2006). Muscle architecture and the physiological properties of muscle fiber are important in the evaluation of muscle capacity. With few exceptions, muscle mass and volume distribution are considered key physical parameters in avian myology, controlling flight (Fisher 1946; Owre 1967). Additional studies are needed to investigate the relationship between fiber-type distribution and muscle function (e.g., Meyers 1992; Torrella et al. 1998; Meyers and Stakebake 2005; Corvidae et al. 2006; Welch and Altshuler 2009). Mass, volume and the type of fiber substantially affect the contractile properties of a muscle. However, more than any other factor, muscle architecture predicts muscle function (Lieber and Fridén 2000; Ward et al. 2009; Lieber and Ward 2011). The importance of muscle fiber architecture has long been recognized and related studies have been widely reported in human and other mammals (Sacks and Roy 1982; Payne et al. 2005, 2006; Williams et al. 2007, 2008; Eng et al. 2008; Channon et al. 2009; Rupert et al. 2014), but seldom in birds. Report on the hind limb of an ostrich by Smith et al. (2006) may have been the first comprehensive research on avian muscle architecture. More work, with a special focus on the functional relationship between muscle architecture and flight styles, is needed (Dial 1992a).
Skeletal muscle architecture is defined as the arrangement of muscle fibers within a muscle (Gans 1982; Sacks and Roy 1982). The two most important architectural parameters are the physiological cross-sectional area (PCSA) and muscle fiber length (Lieber and Fridén 2000). The PCSA of a muscle is the only architectural parameter that is directly proportional to force generation, whereas muscle excursion and velocity are directly proportional to muscle fiber length. A greater serial sarcomere count (i.e., greater fiber length) leads directly to a larger muscle excursion, because serial excursions of individual sarcomeres are additive (Lieber and Ward 2011). Thus, long fibers are predicted to operate over a relatively wide range of muscle lengths, which can achieve greater velocities compared with shorter-fibered muscles. Due to these direct structure-function correlations, architectural features will undoubtedly reflect the functional properties and specializations of different muscles.
The pectoralis and supracoracoideus play dominant roles in bird flight and are the most widely studied of the forelimb muscles. Electromyographic (EMG) data indicate that intrinsic muscles of the wing contribute little additional mechanical power for flight, but are important in modulating wing orientation and controlling wing shape (Dial 1992a, 1992b; Biewener 2011). Due to the difficulty of in vivo force measurements for smaller muscles located more distally in the wing, the roles of these muscles in adjusting the wing, as well as their functional specializations, remain largely unknown (Biewener 2011). Given this circumstance, analysis of muscle architecture can play an important role in evaluating the role of muscles. China is particularly rich in pheasants and their relatives, with the result that these receive more attention than any other group. The Golden Pheasant (Chrysolophus pictus) is an endemic pheasant of China, but with their number decreasing (Lei and Lu 2006). The flight of this species, as well as that of other phasianids involves an explosive take-off followed by a rapid and swift flapping flight (Askew and Marsh 2002). Many investigations have focused on the power output and function of wing muscles during non-steady flight (Dial 1992a, 1992b; Tobalske and Dial 2000; Askew et al. 2001; Askew and Marsh 2002). In this study we have attempted to quantify forelimb muscles architecture in the Golden Pheasant, with an emphasis on the brachial, antebrachial and manual segments and their varying functions in adjusting wing shape. An understanding of muscle architectural specialization illuminates the functional features of the different muscles used during flight and may provide additional information for further biomechanical and in vivo investigations.
Methods
Five adult Golden Pheasants [three females, two males; mass 422±95.8 g (mean±SD)] were obtained from an accredited local farm for use in this study, killed by decapitation. The project was approved by the Animal Care and Ethics Committee of Capital Normal University. After the birds were sacrificed, each limb was skinned and individual muscles were identified, exposed and cleared of fascia. The muscles were then systematically removed and detailed dissections of muscle-tendon architecture were carried out. Muscle architecture was determined from methods described by Smith et al. (2006). Muscle mass measurements were obtained with an electronic scale (Ohaus, USA) to the nearest 0.0001 g, while lengths were measured with digital calipers (Workzone, Germany) to the nearest 0.01 mm. Muscle belly length was measured as the length from the most proximal fibers to the most distal fibers. Muscle volume was calculated by dividing muscle mass by muscle density (1.06 g∙cm-3; Mendez and Keys 1960; Brown et al. 2003) and its physiological cross-sectional area (PCSA) was then determined by dividing muscle volume by its mean fascicle length. To obtain fascicle length, the collagen between the muscle fibers was gradually dissolved in nitric acid (30% HNO3) for about 24 h and then the tissue was immersed in a 50% glycerol solution. At least five measurements of fascicle length were taken from randomly distributed areas and depths within the muscle belly. The maximum isometric force of a muscle, Fmax, was estimated by multiplying PCSA by the maximum isometric stress of a vertebrate skeletal muscle (0.3 MPa; Wells 1965). Pennation angles were not included in our measurements, because muscle bellies in most of the forelimb muscles are directly attached to the skeleton, without forming tendons of insertion. As well, among muscles with an insertion tendon, nearly all angles are smaller than 10°; the cosine of a 10° angle is very close to one and would thus have little effect on estimations of PCSA.
For gross comparison, muscles were assigned to six functional groups: i.e., brachial depressors/elevators, antebrachial extensors/flexors, antebrachial depressors/elevators, manual extensors/flexors, manual depressors/elevators and manual intrinsics. For each functional muscle group, the sum of the separate muscle PCSAs and the total force were combined to result in one value for each group; the fascicle length was averaged among the containing muscles of that group. One way ANOVA was performed within each functional group. Functions of individual muscles have not been previously published for this species and are, therefore, based on anatomical positioning, our personal observations and references from George and Berger (1966).
Results
General features
All 47 previously recognized muscles (Zhang and Yang 2013) were identified in the pectoral limb of the Golden Pheasant. The corresponding architectural data are presented in Table 1. On average, the unilateral forelimb muscle mass of the Golden Pheasant accounts for 12.00%±1.56% (mean±SD) of body mass, corresponding to 51.74 g of muscle per forelimb. Muscles were assigned to four groups according to their location; the distribution of muscle mass exhibited a sharp reduction from the proximal to the distal (Figure 1). Extrinsic muscles, brachial muscles, antebrachial muscles and manual muscles constitute 84.98%, 8.81%, 5.94% and 0.33%, respectively, of the total forelimb muscle mass. The pectoralis (PT), supracoracoideus (SP) and scapulohumeralis caudalis (SHC) are the three largest muscles of the forelimb. PT accounts for 13.4% of the total body mass and 55.86% of the total forelimb muscle mass. The corresponding data for SP are 3.9% and 16.31% and for SHC 1.3% and 5.33%. The largest brachial muscle was triceps brachii, accounting for 4.63% of the total forelimb muscle mass, closely followed by biceps brachii (BB, 1.66%) and deltoideus major (DMA, 1.41%). Triceps brachii is composed of two distinct heads, the humeral and scapular, with the humeral head (TH, 1.331±0.490 g) slightly larger than the scapular head (TS, 1.076±0.439 g). The extensor metacarpi radialis (EMR) and flexor carpi ulnaris (FCU) muscles form the bulk of the antebrachial group, weighing 0.614±0.284 g and 0.469±0.293 g, respectively, corresponding to 1.17 and 0.87% of the total forelimb muscle mass. Smallest were the distal manual muscles, which include the flexor alulae (FA, 0.004±0.002 g, 0.008%), the extensor brevis alulae (EBA, 0.007±0.005 g, 0.014%) and the flexor digiti minoris (FDMI, 0.011±0.006 g, 0.020%).
Table
1.
Architectural properties of forelimb muscles in the Golden Pheasant
Among muscles with an insertion tendon, tendon lengths were obtained only from those that were discernible. The proportional lengths of muscle belly and tendon lengths are shown in Figure 2. Most tendons in the distal limb are comparatively longer than those in the proximal limb and exceed belly lengths.
Figure
2.
Comparison between tendon length and muscle belly length for both the proximal (dark red and dark blue) and distal (light red and light blue) forelimb muscles of the Golden Pheasant.
The distribution of fascicle lengths showed a general trend, with proximal muscles having longer fascicles and distal muscles relatively short fascicles. The pectoralis and supracoracoideus had the longest mean fascicle lengths (2.44 cm and 2.33 cm, respectively), followed closely by the latissimus dorsi, deltoideus major, tensor propatagialis and scapulohumeralis caudalis. Intrinsic manual muscles displayed the shortest fascicle lengths, ranging from 0.16 to 0.44 cm. Among the intrinsics, the abductor and adductor of the alular digit were relatively high in this parameter.
The pectoralis muscle had, on average, the largest PCSA (11.15 cm2), thus yielding the highest force-producing capacity of all the forelimb muscles (Fmax=334.55 N), followed by the supracoracoideus (3.63 cm2, 108.95 N). PCSAs of most of the intrinsics of the manus, i.e., latissimus dorsi pars cranialis, scapulohumeralis cranialis, serratus superficialis pars cranialis and brachialis, were the smallest, at less than 0.1 cm2.
Comparisons between functional groups
The fascicle length and PCSA of six functional groups are shown in Table 2. A significant difference (p < 0.05) was observed between the antebrachial depressors and elevators for PCSA and total force. The difference in PCSA and total force between the intrinsics of the alular digit and major digit was also significant (p < 0.05).
Disparities in architectural properties and mechanical function within a synergic group, or between different functional groups, are shown in Figure 3. The antebrachial extensors were characterized by high force-producing capacities, whereas the flexors showed more diversification in their fundamental design: FCU and BB would be expected to govern function because of their large PCSAs, while TP has the capacity to perform a large excursion. Considering the depressors (or pronators) vs. elevators (supinators) comparison, the other antagonistic groups of the antebrachium, the former possessed a significantly larger PCSA and relatively longer FL than the latter. The FCU appeared to control the flexion of the manus in force production. Extension of the manus tended to be more complicated than flexion for simultaneously possessing a large PCSA muscle (EMR) and a long FL muscle (ELA), features that suggest a design predicated on both force and speed. All intrinsic muscles of the manus are indicated on the bottom of the left-hand side of Figure 3 (low PCSA, short fascicles). They differ anatomically in that the muscles of the major digit are characterized by large PCSAs, whereas the muscles in the alular digit are remarkable for their long fascicle lengths.
Figure
3.
Scatter graph of fascicle length and physiological cross-sectional areas (PCSAs) of muscles in the forelimb of the Golden Pheasant.
Along with certain mammals and birds, such as horses and ostriches (Payne et al. 2005; Smith et al. 2006), the distribution of muscle mass throughout the Golden Pheasant forelimb demonstrated a proximal-to-distal reduction. This design minimizes the moment of inertia during locomotion (Hildebrand 1988), which, in turn, conserves metabolic energy (Steudel 1996). The tendon in the distal forelimb segment of the Golden Pheasant was relatively longer than that found in the proximal. This extra length enables muscles to control distal movements of the wing without the burden of extra muscle mass. Possessing a small and lightweight distal segment (Biewener 2011) provides a distinct advantage by decreasing limb inertia during flight. The ability of tendons to stretch and recoil enables storage and recovery of elastic energy, while allowing muscle fibers to sustain high forces (Roberts 2002). Longer tendons in the distal forelimb enhance muscle performance by increasing contraction efficiency and reducing metabolic costs.
As the primary wing depressor and elevator, the pectoralis and supracoracoideus are the most widely studied of the forelimb muscles. In the Golden Pheasant, these two muscles possess the largest mass, PCSA and proportion of all the muscles in the forelimb. As expected, they also possess the longest fascicle lengths. Greenwalt (1962) predicted that the pectoralis muscle of a volant species should constitute 15.5% of the total body mass of a bird. In the Golden Pheasant, this muscle comprises 13.4% of total body mass. Regarding the supracoracoideus, this muscle represents about 1.6% of the total body mass in volant birds and most non-diving birds, 4%-5% in wing-propelled diving birds (e.g., Atlantic Puffin) and 10%-12% in penguins (Greenwalt 1962; Poore et al. 1997; Kovacs and Meyers 2000). Our results show that the supracoracoideus in the Golden Pheasant accounts for 3.9% of the total body mass of this species. The relatively large supracoracoideus in alcids and other wing-propelled diving birds most likely evolved to raise the wing against the resistive drag of water (Kovacs and Meyers 2000). The pheasants use high-frequency, high-amplitude wing beats during their explosive take-off flights and these attributes probably create a high inertial power requirement for elevating the wing. In the Golden Pheasant, it is likely that the supracoracoideus is large to meet this inertial-work or inertial-power requirement. A long fascicle results in greater excursion length, whereas PCSA corresponds to force production. The long fascicle and large PCSA of the pectoralis and supracoracoideus enable powerful upstrokes and downstrokes through a large excursion to achieve sufficient aerodynamic lift, particularly during takeoff and vertical ascending flights (Biewener 2011).
Previous work (Dial 1992a; Berg and Biewener 2010) demonstrated that the brachial and antebrachial muscles act primarily as joint stabilizers and are not essential for normal extension and flexion of the wing during level flapping flights. However, during non-steady flights (e.g., takeoffs and landings), these muscles contribute to the performance of the wing by acting as an aerofoil, modulating wing orientation and wing shape (Dial 1992a, 1992b; Biewener 2011). In this study, we have demonstrated differences in architectural design within antagonistic groups of the antebrachial muscles (Table 2). For example, antebrachial elevators vs. depressors present significant differences in total PCSA and estimated isometric force (p < 0.05). Similar differences were also observed between intrinsic muscles of the major and alular digits, which have architectural features that facilitate force production (major digits) and excursion (alular digit). Pronounced development of the antebrachial depressors (pronator superficialis, pronator profundus and ectepicondylo ulnaris) suggests that ventrally rotating the distal half of the wing should profoundly affect shape change and orientation modulation during non-steady flights; these muscles are evidently capable of providing increased thrust for acceleration during takeoff and vertical ascending flights (Biewener 2011). A similar trend was also found in pigeons, where the pronator superficialis exhibited biphasic activities with EMG intensities at their maximum during takeoff and ascending flights (Dial 1992b). Three birds of prey (Cooper's Hawk Accipiter cooperii, Osprey Pandion haliaetus and Red-tailed Hawk Buteo jamaicensis) also exhibit these muscle-induced phenomena, which may explain observed differences in flight mode and hunting behavior (Corvidae et al. 2006). The manus intrinsics (Figure 3) may be related to joint stabilization or the execution of precision movements (Williams et al. 2008; Channon et al. 2009). The major digit provides support for the outer primaries that control forward thrust and aerodynamic performance, particularly during flapping flights (Combes and Daniel 2001; Swaddle and Lockwood 2003). The major digit intrinsics, with their greater PCSAs and force generation capability, may help stabilize the wing and provide powerful support for the primary feathers. The alula, or bastard wing, is a high lift device located at the leading edge of the wing that allows birds to fly at an acute attack angle and at a lower speed without stalling (Gill 1995; Alvarez et al. 2001). It features 3 to 5 small flight feathers originating from the first digit and moves independently of the rest of the wingtip. Four muscles attach to the alular digit and control the position of the alula; among them, the adductor and abductor appear to be dominant and more effective functionally due to their significantly longer fascicles. Their architectural properties are designed for excursion and velocity, as muscles with relatively long fibers operate over a large range of muscle lengths and can achieve faster velocities compared with a shorter-fibered muscle (Ward et al. 2009). This may imply that adjustment of the alula is paramount for rapid adduction and abduction during flight in the Golden Pheasant.
Our results also revealed that muscle architecture varies widely within synergic groups (Figure 3, Table 2). The flexors of the manus, for example, are composed of six different muscles: i.e., flexor carpi ulnaris, flexor digitorum profundus, flexor digitorum superficialis, extensor carpi ulnaris, ulnometacarpalis ventralis and ulnometacarpalis dorsalis. They all contribute to flexion of the manus. The flexor carpi ulnaris (FCU), with the largest PCSA at nearly 8 times that of the flexor digitorum superficialis, generates very high forces and acts as the functionally dominant muscle in this group. Within the manual extensors group, extensor metacarpi radialis was designed for optimal force production, whereas extensor longus alulae evolved for fast velocity. These results are consistent with Dial's observation (1992a) that the extensor metacarpi radialis and flexor carpi ulnaris exhibited their greatest EMG activity during non-steady flights, indicating that the manus extension is significantly more complicated than flexion.
Competing interests
The authors declare that they have no competing interests.
Authors' contributions
ZZ designed the experiments, and YY and HW conducted the experiments. ZZ, HW and YY analyzed the data and wrote the paper. All authors read and approved the final manuscript.
Acknowledgments
We thank Guangdi Si for her help with laboratory work. This work was supported by the National Natural Science Foundation of China (30870263, 31272259).
Alonso JC, Bautista LM, Alonso JA. Family-based territoriality vs flocking in wintering common cranes Grus grus. J Avian Biol. 2004;35: 434-44.
Ashmole NP, Tovar SH. Prolonged parental care in royal terns and other birds. Auk. 1968;85: 90-100.
Barlow M. Movements of Caspian Terns (Sterna caspia) from a colony near Invercargill, New Zealand, and some notes on their behaviour. Notornis. 1998;45: 193-220.
Becker PH, Schmaljohann H, Riechert J, Wagenknecht G, Zajková Z, González-Solís J. Common Terns on the East Atlantic Flyway: temporal-spatial distribution during the non-breeding period. J Ornithol. 2016;157: 927-40.
Black JM. Fitness consequences of long-term pair bonds in barnacle geese: monogamy in the extreme. Behav Ecol. 2001;12: 640-5.
Bried J, Jouventin P. Site and mate choice in seabirds: an evolutionary approach. In: Schreiber EA, Burger J, editors. Biology of marine birds. CRC Marine Biology Series, 1. Boca Raton: CRC Press; 2001. p. 263-305.
Bried J, Jiguet F, Jouventin P. Why do Aptenodytes penguins have high divorce rates? Auk. 1999;116: 504-12.
Bried J, Pontier D, Jouventin P. Mate fidelity in monogamous birds: a re-examination of the Procellariiformes. Anim Behav. 2003;65: 235-46.
Busse K. Untersuchungen zum Ehe-, Familien- und Sozialleben der Küstenseeschwalbe (Sterna paradisaea PONT) mit besonderer Berücksichtigung des langzeitlichen Wandels der individuellen Beziehungen. Ökologie Der Vögel. 1983;5: 73-110.
Cabot D, Nisbet I. Terns. 1st ed. London: Collins; 2013.
Carroll G, Cox M, Harcourt R, Pitcher BJ, Slip D, Jonsen I. Hierarchical influences of prey distribution on patterns of prey capture by a marine predator. Funct Ecol. 2017;31: 1750-60.
Choudhury S. Divorce in birds: a review of the hypotheses. Anim Behav. 1995;50: 413-29.
Cockburn A. Prevalence of different modes of parental care in birds. Proc R Soc B Biol Sci. 2006;273: 1375-83.
Covas R, Griesser M. Life history and the evolution of family living in birds. Proc R Soc B Biol Sci. 2007;274: 1349-57.
Cramp S. Handbook of the birds of Europe, the Middle East and North Africa. The Birds of Western Palearctic. Vol. IV. Terns to woodpeckers. Oxford: Oxford University Press; 1985.
Davis SE, Maftei M, Mallory ML. Migratory connectivity at high latitudes: Sabine's gulls (Xema sabini) from a colony in the Canadian high arctic migrate to different oceans. PLoS ONE. 2016;11: e0166043.
Egevang C, Stenhouse IJ, Phillips RA, Petersen A, Fox JW, Silk JRD. Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proc Natl Acad Sci USA. 2010;107: 2078-81.
Fayet AL, Shoji A, Freeman R, Perrins CM, Guilford T. Within-pair similarity in migration route and female winter foraging effort predict pair breeding performance in a monogamous seabird. Mar Ecol Prog Ser. 2017;569: 243-52.
Feare CJ. Post-fledging parental care in Crested and Sooty Terns. Condor. 1975;77: 368-70.
Fijn RC, Hiemstra D, Phillips RA, van der Winden J. Arctic Terns Sterna paradisaea from The Netherlands migrate record distances across three oceans to Wilkes Land, East Antarctica. Ardea. 2013;101: 3-12.
Fletcher KL, Hamer KC. Sexing terns using biometrics: the advantage of within-pair comparisons: within-pair comparisons substantially improve the accuracy of sexing from biometrics for two congeneric species of seabird with monomorphic plumage and soft-tissue colouration. Bird Study. 2003;50: 78-83.
Flodin LÅ, Blomqvist D. Divorce and breeding dispersal in the dunlin Calidris alpina: support for the better option hypothesis? Behaviour. 2012;149: 67-80.
Forslund P, Larsson K. The effect of mate change and new partner's age on reproductive success in the barnacle goose, Branta leucopsis. Behav Ecol. 1991;2: 116-22.
González-Solís J, Becker PH, Wendeln H. Divorce and asynchronous arrival in common terns, Sterna hirundo. Anim Behav. 1999;58: 1123-9.
Hedenström A, Åkesson S. Ecology of tern flight in relation to wind, topography and aerodynamic theory. Philos Trans R Soc B Biol Sci. 2016;371: 20150396.
Herbert-Read JE. Understanding how animal groups achieve coordinated movement. J Exp Biol. 2016;219: 2971-83.
Hijmans RJ, Williams E, Vennes C. geosphere: spherical trigonometry. R package geosphere version 1.5-10. 2019. . Accessed 12 June 2021.
Holland MM, Smith JA, Everett JD, Vergés A, Suthers IM. Latitudinal patterns in trophic structure of temperate reef-associated fishes and predicted consequences of climate change. Fish Fish. 2020;21: 1092-108.
Jeschke JM, Wanless S, Harris MP, Kokko H. How partnerships end in guillemots Uria aalge: chance events, adaptive change, or forced divorce? Behav Ecol. 2007;18: 460-6.
Johnsgard PA, Mangelsen TD. A chorus of cranes: the cranes of North America and the world. 1st ed. Boulder: University Press of Colorado; 2015.
Johnston VH, Ryder JP. Divorce in larids: a review. Colon Waterbirds. 1987;10: 16-26.
Kubo A, Takahashi A, Thiebot JB, Watanuki Y. Rhinoceros Auklet pair-mates migrate independently but synchronize their foraging activity during the pre-laying period. Ibis. 2018;160: 832-45.
López-Idiáquez D, Vergara P, Fargallo JA, Martínez-Padilla J. Providing longer post-fledging periods increases offspring survival at the expense of future fecundity. PLoS ONE. 2018;13: e0203152.
Mostello CS, Nisbet ICT, Oswald SA, Fox JW. Non-breeding season movements of six North American Roseate Terns Sterna dougallii tracked with geolocators. Seabird. 2014;27: 1-21.
Müller MS, Massa B, Phillips RA, Dell'Omo G. Seabirds mated for life migrate separately to the same places: behavioural coordination or shared proximate causes? Anim Behav. 2015;102: 267-76.
Nisbet ICT, Montoya JP, Burger J, Hatch JJ. Use of stable isotopes to investigate individual differences in diets and mercury exposures among common ternsSterna hirundo in breeding and wintering grounds. Mar Ecol Prog Ser. 2002;242: 267-74.
Nisbet ICT, Szczys P, Mostello CS, Fox JW. Female Common Terns Sterna hirundo start autumn migration earlier than males. Seabird. 2011;24: 103-7.
Pöysä H. Group foraging in patchy environments: the importance of coarse-level local enhancement. Ornis Scand. 1992;23: 159-66.
Preddey JM. Post-fledging parental care of a juvenile New Zealand fairy tern (Sterna nereis davisae). Notornis. 2008;55: 159-61.
R Core Team. R: a language and environment for statistical computing. Vienna: R Found. Stat. Comput; 2019. . Accessed 7 Oct 2019.
Rakhimberdiev E, Winkler DW, Bridge E, Seavy NE, Sheldon D, Piersma T, et al. A hidden Markov model for reconstructing animal paths from solar geolocation loggers using templates for light intensity. Mov Ecol. 2015;3: 25.
Rakhimberdiev E, Senner NR, Verhoeven MA, Winkler DW, Bouten W, Piersma T. Comparing inferences of solar geolocation data against high-precision GPS data: annual movements of a double-tagged black-tailed godwit. J Avian Biol. 2016;47: 589-96.
Rakhimberdiev E, Saveliev A, Piersma T, Karagicheva J. FLightR: an R package for reconstructing animal paths from solar geolocation loggers. Methods Ecol Evol. 2017;8: 1482-7.
Redfern CPF, Bevan RM. Use of sea ice by arctic terns Sterna paradisaea in Antarctica and impacts of climate change. J Avian Biol. 2020a;51: e02318.
Redfern CPF, Bevan RM. Overland movement and migration phenology in relation to breeding of Arctic TernsSterna paradisaea. Ibis. 2020b;162: 373-80.
Redfern C, Kinchin-Smith D, Morrison P. Little-endian Arctic Tern and Roseate Tern in Northumberland. Br Birds. 2019;112: 357-9.
Redfern CPF, Kinchin-Smith D, Newton S, Morrison P, Bolton M, Piec D. Upwelling systems in the migration ecology of Roseate Terns (Sterna dougallii) breeding in northwest Europe. Ibis. 2021;163: 549-65.
Sánchez-Macouzet O, Rodríguez C, Drummond H. Better stay together: pair bond duration increases individual fitness independent of age-related variation. Proc R Soc B Biol Sci. 2014;281: 20132843.
Sankey DWE, Portugal SJ. When flocking is costly: reduced cluster-flock density over long-duration flight in pigeons. Sci Nat. 2019;106: 47.
Scott DK. Functional aspects of prolonged parental care in Bewick's swans. Anim Behav. 1980;28: 938-52.
Strandberg R, Alerstam T. The strategy of fly-and-forage migration, illustrated for the osprey (Pandion haliaetus). Behav Ecol Sociobiol. 2007;61: 1865-75.
Sutton GJ, Hoskins AJ, Arnould JPY. Benefits of group foraging depend on prey type in a small marine predator, the little penguin. PLoS ONE. 2015;10: e0144297.
Thiebot JB, Bost CA, Dehnhard N, Demongin L, Eens M, Lepoint G, et al. Mates but not sexes differ in migratory niche in a monogamous penguin species. Biol Lett. 2015;11: 20150429.
Watson MJ, Spendelow JA, Hatch JJ. Post-fledging brood and care division in the roseate tern (Sterna dougallii). J Ethol. 2012;30: 29-34.
Wiley EM, Ridley AR. The benefits of pair bond tenure in the cooperatively breeding pied babbler (Turdoides bicolor). Ecol Evol. 2018;8: 7178-85.
Withers GD. A study of the population and behaviour of the Arctic Tern. 1973. . Accessed 12 June 2021.
Lin Wang, Mingjie Liu, Zihui Zhang. Reversed sexual dimorphism in the leg muscle architecture of the Eurasian sparrowhawk. The Anatomical Record, 2023, 306(2): 437.
DOI:10.1002/ar.25066
2.
Xinxin Liang, Mingjie Liu, Chenxi Ying, et al. Myological variation in the hindlimb of three raptorial birds in relation to foraging behavior. Avian Research, 2022, 13: 100053.
DOI:10.1016/j.avrs.2022.100053
3.
James Charles, Roger Kissane, Tatjana Hoehfurtner, et al. From fibre to function: are we accurately representing muscle architecture and performance?. Biological Reviews, 2022, 97(4): 1640.
DOI:10.1111/brv.12856
4.
Lin Wang, Xinsen Wei, Xinxin Liang, et al. Ontogenetic changes of hindlimb muscle mass in Cabot's tragopan (Galliformes, Phasianidae) and their functional implications. The Anatomical Record, 2021, 304(12): 2841.
DOI:10.1002/ar.24609
5.
Fernanda Bribiesca-Contreras, Ben Parslew, William I. Sellers. Functional morphology of the forelimb musculature reflects flight and foraging styles in aquatic birds. Journal of Ornithology, 2021, 162(3): 779.
DOI:10.1007/s10336-021-01868-y
6.
Meg L. Martin, Kenny J. Travouillon, Patricia A. Fleming, et al. Review of the methods used for calculating physiological cross-sectional area (PCSA) for ecological questions. Journal of Morphology, 2020.
DOI:10.1002/jmor.21139
7.
Nadezhda V. Kryukova, Alexander N. Kuznetsov. Suboccipital muscle of sharpnose sevengill shark Heptranchias perlo and its possible role in prey dissection. Journal of Morphology, 2020.
DOI:10.1002/jmor.21142
8.
Fernanda Bribiesca‐Contreras, Ben Parslew, William I. Sellers. A Quantitative and Comparative Analysis of the Muscle Architecture of the Forelimb Myology of Diurnal Birds of Prey (Order Accipitriformes and Falconiformes). The Anatomical Record, 2019, 302(10): 1808.
DOI:10.1002/ar.24195
9.
S P Sullivan, F R McGechie, K M Middleton, et al. 3D Muscle Architecture of the Pectoral Muscles of European Starling (Sturnus vulgaris). Integrative Organismal Biology, 2019, 1(1)
DOI:10.1093/iob/oby010
10.
Ashley M. Heers, Jeffery W. Rankin, John R. Hutchinson. Building a Bird: Musculoskeletal Modeling and Simulation of Wing-Assisted Incline Running During Avian Ontogeny. Frontiers in Bioengineering and Biotechnology, 2018, 6
DOI:10.3389/fbioe.2018.00140
11.
Daria Razmadze, Aleksandra A. Panyutina, Nikita V. Zelenkov. Anatomy of the forelimb musculature and ligaments ofPsittacus erithacus(Aves: Psittaciformes). Journal of Anatomy, 2018, 233(4): 496.
DOI:10.1111/joa.12861
12.
H. Wang, J. Yan, Z. Zhang. Sexual dimorphism in jaw muscles of the Japanese sparrowhawk (Accipiter gularis ). Anatomia, Histologia, Embryologia, 2017, 46(6): 558.
DOI:10.1111/ahe.12309
13.
Fernanda Bribiesca-Contreras, William I. Sellers. Three-dimensional visualisation of the internal anatomy of the sparrowhawk (Accipiter nisus) forelimb using contrast-enhanced micro-computed tomography. PeerJ, 2017, 5: e3039.
DOI:10.7717/peerj.3039
DownLoad:
Email Alerts
RSS Feeds