Osteohistological variations in the Antarctic penguin Pygoscelis adeliae (Aves, Sphenisciformes)

doi:10.21203/rs.3.rs-2622108/v1

Download PDF

Research Article

Osteohistological variations in the Antarctic penguin Pygoscelis adeliae (Aves, Sphenisciformes)

https://doi.org/10.21203/rs.3.rs-2622108/v1

This work is licensed under a CC BY 4.0 License

Journal Publication

published 18 Jul, 2023

Read the published version in Polar Biology →

You are reading this latest preprint version

To analyze the osteohistological variations between adult individuals of Pygoscelis adeliae, histological sections of the mid-level of the shaft of different bones (humerus, radius, ulna, carpometacarpus, femur, tibiotarsus, tarsometatarsus and ribs) of a female and a male, were compared. The results indicate that, at the microanatomical level, the sections present a compact tissue with a reduced (or null) medullary cavity and a high bone density resulting from the internal compaction of the tissues. At the histological level, three tissue regions, defined by their bone matrix, level of organization of the vascular channels, and the degree of compaction, can be identified. However, sexual differences and variations in the microstructure and histology along the skeleton were found in the penguin Pygoscelis adeliae. A medullary cavity defined by an inner circumferential system appears in the male, whereas in the female, a remaining medullary cavity without the development of an inner circumferential layer, a lower degree of bone compaction, the presence of medullary tissue, and intertrabecular spaces, was observed. These results are consistent with reports of medullary bone in females from other groups of birds and provided an assistant criterion for the differentiation of sexes.

Adélie Penguin

Spheniscidae

bone microanatomy

bone histology

sexual differences

Antarctic Peninsula

The Sphenisciformes (penguins) are an order of flightless seabirds that exhibit the most extreme specializations for wing-propelled diving (Stonehouse 1975; Simpson 1976). The eighteen extant species are organized into six genera (Winkler et al. 2020) and exclusively distributed following the cold water currents of the southern seas (Martínez 1992). In particular, the genus Pygoscelis (Wagler 1832) comprises three living species: Pygoscelis adeliae (Hombron and Jacquinot 1841), P. antarctica, and P. papua (Forster 1781), plus the three fossil species P. tyreei from New Zealand (Simpson 1972), P. calderensis (Acosta Hospitaleche et al. 2006)d grandis (Walsh and Suárez 2006) from Chile.

Breeding aggregations of Pygoscelis adeliae occur in ice-free areas in the Ross Sea, along the west coasts of the Antarctic Peninsula, and on the Scotia Arc islands (Trathan and Ballard 2015). Adélie penguins breed in large colonies, maintain the same reproductive mate for successive years, and exhibit recurrent use of their nests (Trathan and Ballard 2015). The reproductive cycle comprises a migratory stage (April/August), after which they return to the colony for the reproductive period (September/October), spending the following months laying eggs and raising chicks until mid-January (Emmerson et al. 2011). Then begins the period of independence of the juveniles until the first moult in late February and early March (Emmerson et al. 2011). The mean reproductive age of the first reproduction is 4.7-5.0 years for females and 6.2–6.8 for males (Ainley et al. 1983).

Adults females and males are morphologically similar, although females are usually smaller (Ainley and Emison 1972; Scolaro et al. 1991; Kerry et al. 1992). In the same way, males have greater body masses and also longer and deeper bills than females (Polito et al. 2012; Fattorini and Olmastroni 2021). Despite the patterns of both external and skeletal morphological variation established for pygoscelid penguins (Acosta Hospitaleche and Tambussi 2006; Jennings et al. 2016; Fattorini and Olmastroni 2021), bone microstructure studies are still scarce, not only in Pygoscelis (Meister 1962; Wilson and Chin 2014) but also in all penguins (e.g. Chinsamy et al. 1998; de Margerie et al. 2004; Cerda et al. 2015; Ksepka et al. 2015; Garcia Marsà et al. 2020). In this regard, only the microstructure of the femur and tibiotarsus of adult specimens of Pygoscelis adeliae have been described (Meister 1962; Wilson and Chin 2014). From a histological point of view, these contributions mention the presence of high-density bone tissue, with three differentiated concentric regions. A cortical region (outer zone) composed of a circumferential layer with the presence of Volkmann's canals, a perimedullary region (middle zone) with secondary osteons organized in longitudinal vascular channels, and a medullary region (inner zone) composed of spongy tissue with a large number of trabeculae surrounded by lamellar tissue (Meister 1962). Furthermore, the dominance of longitudinal vascular channels and a few other anastomosed channels in the cortex of the tissue have been observed in this species, resulting in a reticular vascular pattern and the absence of growth lines or growth cycles (Wilson and Chin 2014). According to that, it is necessary to extend the analysis to other skeletal elements to contemplate their osteohistological variability comprehensively.

The present contribution aims to improve the acknowledgment of the microstructure and histology of the Pygoscelis adeliae bones. According to that, the osteohistological variations between adult individuals were analyzed from multi-elemental histological sections, performed at the level of the mid-shaft in the humerus, radius, ulna, carpometacarpus, femur, tibiotarsus, tarsometatarsus, and (vertebral and sternal) ribs. A male and a female from the same reproductive colony were compared here.

The specimens come from Bahía Esperanza, Trinidad Peninsula (Antarctica), and have been housed in the osteological collection of the Ornithology Section of the Vertebrate Zoology Division of the Museo de La Plata (MLP-O) in Argentina. The humerus, radius, ulna, carpometacarpus, femur, tibiotarsus, tarsometatarsus, and (vertebral and sternal) ribs of a female that was found dead just before laying eggs (MLP-O 15137) and a male (MLP-O 15177) of Pygoscelis adeliae were examined (Fig. 1). Eighteen thin sections were prepared at the Laboratory of Thin Sections of the Instituto de Investigación en Paleobiología y Geología (IIPG). Accordingly, cross-sections of each specimen at the level of the mid-shaft were made using the protocol proposed by Chinsamy and Raath (1992). The slides obtained were analyzed with a petrographic microscope (ZEISS Axio Imager) under the plane and cross-polarized light. Images of each thin section were captured by a digital camera (ZEISS Axiocam 105) and processed with Adobe Photoshop 2020 and Adobe Illustrator 2022

Microanatomy

All the elements analyzed (humeri, radi, ulnae, carpometacarpi, femora, tibiotarsi, tarsometatarsi, vertebral and sternal ribs) show a similar microanatomical pattern for both sexes (Fig. 2). This is characterized by a compact tissue that preserves a reduced (or null) medullary cavity with some intertrabecular spaces towards the medullary region. In the female (MLP-O 15137), a greater development of intertrabecular spaces and a lower degree of bone compaction than in the male (MLP-O 15177) were observed. The sections of the femora, tibiotarsi, tarsometatarsi, vertebral, and sternal ribs of male present a well-defined medullary cavity delimited by an inner circumferential layer, whereas, in the female, a remaining medullary cavity without the development of an inner circumferential layer was observed.

Histology

Three regions (cortical, perimedullary, and medullary), defined by their bone matrix, organization level of the vascular channels, and compaction degree, are recognized in both specimens. In the cortical region (Fig. 3a, 3b), all sections exhibit a thin layer of lamellar tissue, mostly avascular, with lines of arrested growth (LAGs) that vary according to gender and skeletal element. One LAG was observed in the radi, tibiotarsi, and (vertebral and sternal) ribs, but two in the femora and tarsometatarsi of both specimens. However, the humeri, ulnae, and carpometacarpi present two LAGs in males and one in females.

In the perimedullary region (Fig. 3c, 3d), all sections are composed of secondary osteons defined by clear cementing lines arranged mainly in a longitudinal vascular pattern. Nevertheless, some channels with a reticular distribution are observed (except for the vertebral and sternal ribs). In the ribs, the vascular pattern is clearly longitudinal. Osteons may present Volkmann's channels that remodel the primary tissue. Although, under polarized light the bone matrix cannot be distinguished from the vestiges of the primary tissue, this is evidenced by the morphology of the osteocyte lacunae. These lacunae, derived from static osteogenesis, are circular and larger than the lacunae derived from dynamic osteogenesis, which are smaller, discoidal, and oriented according to the distribution of the fibres.

In the medullary region (Fig. 3e, 3f), the osteohistological differences between the male (MLP-O 15177) and the female (MLP-O 15137) are strongly marked. A secondarily compacted trabecular tissue, which retains some irregular intertrabecular spaces surrounded by lamellar tissue, is observed. The male is characterized by the lower development of intertrabecular spaces and consequently a greater degree of bone compaction. In the particular cases of the femur, tibiotarsi, tarsometatasi, and ribs, a medullary cavity well-defined by an inner circumferential layer was observed in the male. On the other hand, greater development of intertrabecular spaces and a remaining medullary cavity, which is not delimited by an inner circumferential layer, is observed in the female. Likewise, all the female sections have medullary bone surrounding the intertrabecular spaces of the tissue, and in the cavities of the medullary region.

Finally, no Sharpey's fibres were observed in any of these sections.

Sex differences

The results exposed above show that the microanatomy of all the elements analyzed presents a compact tissue at the level of the mid-shaft with some differences between the male and female. In the male, a medullary cavity defined by an inner circumferential system was observed. In the female, a remaining medullary cavity without the development of an inner circumferential layer, with a lower degree of bone compaction, medullary tissue, and intertrabecular spaces were found. In both, bone compaction appears as the result of secondary compaction of the trabecular tissue, but in the male, the thickening of the inner circumferential layer is added. These specialized patterns, named osteosclerotic, that reduce the tissue cavities producing a compact and heavy bone structure, have been widely recognized in penguins (de Ricqlès and de Buffrénil 2001; Ksepka et al. 2008; Ksepka et al. 2015; Cerda et al. 2015). The tissue compaction, and the thickening of the circumferential layer, have already been defined as specific adaptations to the aquatic environment. It reduces buoyancy, preserves more energy during diving, and improves resistance to bending or torsional loads (de Ricqlès and de Buffrénil 2001; Habib and Ruff 2008; Houssaye 2009; Habib 2010; Houssaye 2013).

The difference in the compaction degree between the male and the female is due to the osteoclastic action that will result in the development of the medullary bone, which serves as a temporary calcium reservoir during egg laying (Bloom et al. 1941; Dacke et al. 1993; Bailleul et al. 2019; Canoville et al. 2019). Likewise, medullary bone was identified in the appendicular and axial bones of the female, reinforcing the concept of a complete skeletal distribution (Bailleul et al. 2019; Canoville et al. 2019). Although medullary bone is used as a marker of reproductive activity or maturation (Bailleul et al. 2019), it is unknown whether it takes place before or after somatic maturation. However, in birds it usually occurs after somatic maturation has been reached (Padian and Woodward 2021).

In future research, it is still necessary to evaluate the histology of female penguins outside the oviposition period to observe if the development of an ICL occurs and then disappears by the osteoclastic intervention (during the egg laying) or if it never developed. Under this criterion, the absence of an ICL in adult females outside the oviposition period could be used as a tool for sexual differentiation in Pygoscelis adeliae and probably in penguins in general, including fossil species, in which the sources of morphological variations are in many cases poorly misunderstood. For example, it is probable that remains referred to different species, like Anthropornis grandis and A. nordenkjöledi, or Palaeeudyptes gunnari and P. arctowski, correspond in fact to females and males of the same species. Successive (qualitative, morphometric, morpho-geometric) analyses have dealt with this issue, without reaching a completely satisfactory result, which allows postulating without further doubts that the remains a single species or two different species in both cases (a further discussion can be found in Acosta Hospitaleche and Reguero 2010, 2014; Jadwiszczak and Acosta Hospitaleche 2013)

Outer circumferential layer in Pygocelis adeliae

Cortical LAGs are rare in extinct and extant groups of birds (e.g. Amprino and Godina 1947; Padian et al. 2001; Turvey et al. 2005; Castanet 2006; Bourdon et al. 2009; Canoville et al. 2022). Castanet (2006) was the first to report the presence of LAGs in penguins, based on the description of the femur of a juvenile Aptenodytes patagonicus. These growth marks were interpreted as the result of the long periods of fasting that this species endures (Castanet, 2006) or as the reflection of the seasonal environment stress (Tutken et al. 2004). Conversely, individuals that develop an azonal bone without interruption of LAGs and with less isotopic variability can be interpreted as migratory organisms (Tutken et al. 2004). To test these, Wilson and Chin (2014) analyzed the osteohistology of pygoscelid penguins contemplating migratory (Pygocelis adeliae, P. antarctica) and non-migratory (P. papua) species, identifying an outer circumferential layer (OCL) and the absence of LAGs in the bone tissue of the three species. Based on that, the absence of growth marks would indicate that the migratory habit is not recorded in the bone tissue in the form of LAGs or zones (Wilson and Chin 2004). Likewise, the presence of an OCL would indicate skeletal maturity within the first year, which is usual in most modern birds (Padian and Woodward 2021), except for the kiwi (Bourdon et al. 2009). In the present work LAGs were identified but occur at the cortical margin within an avascular lamellar matrix. Therefore, this tissue has been interpreted as an OCL. This evidence, added to the bone remodelling degree, we interpret as an indicator of somatic maturity of both individuals.

Vascular patterns

Certain microstructural characteristics are related to habits. Thus, for example, flying birds display high degrees of vascularity with a reticular organization, a thin but compact periosteum, low bone density, and absence (or scant presence) of lines of arrested growth (Hall 1991; Chinsamy 2005). These features reflect the high metabolic rates of the group and its biomechanical properties to take flight. However, when we analyze in detail the microstructure of flightless birds (such as Hesperornis and Patagopteryx), the structural patterns change radically in several ways: it lacks the typical triple-layer structure generally associated with adult modern birds (with an ICL and OCL of the bone surrounding a central tissue of fibrolamellar bone), vascular canals are longitudinally oriented (with some circumferential and radial arrangements) and, distinctive LAGs are developed (e.g. Houde 1987; Chinsamy et al. 1998).

In the individuals analyzed here, the vascular pattern is predominantly longitudinal; however, in the perimedullary region, vascular channels with a reticular distribution pattern are observed. This pattern could be interpreted as a retention of the vascular pattern of their flying ancestors (Raikow et al. 1988) or secondarily caused by bone compaction and remodeling. To test this hypothesis, it is necessary to study specimens in different ontogenetic stages.

Sexual differences and variations in microstructure and histology along the skeleton were found in the penguin Pygoscelis adeliae. The osteosclerotic condition found in humeri, radi, ulnae, carpometacarpi, femora, tibiotarsi, tarsometatarsi, and (vertebral and sternal) ribs are less marked in the female than in the male, as a result of the reabsorption of the osteological tissues. In the male, a medullary cavity defined by an inner circumferential system was observed, while in the female, a remaining medullary cavity without an inner circumferential layer was observed. However, the male and female exhibit a reduced (or null) medullary cavity and a high density due to the internal compaction of the tissues.

As expected, the medullary bone was found only in females. This tissue was recognized in the females of other birds, but the precise morphology in each bone of the skeleton, and the comparison with the homologous elements in the male, represent a novelty result. Thus, we can certainly confirm that it can be used as a tool for the differentiation of females from males in Pygoscelis adeliae and probably in other extant and extinct penguin species.

This work was partially supported by Universidad Nacional de Río Negro PIUNRN 40-A-953, Universidad Nacional de La Plata (N955), Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (PICT 2016 0607) and Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 0096).

Acknowledgements

We thank Mariana Picasso, Luciano Segura, and Diego Montalti (MLP) for access to material, and Juan Ignacio Ison (IIPG) for technician support during thin sections preparation.

Competing Interests: None.

Acosta Hospitaleche C, Chávez M, Fritis O (2006) Pingüinos fósiles (Pygoscelis calderensis sp. nov.) en la Formación Bahía Inglesa (Mioceno Medio-Plioceno), Chile. Rev Geol Chile 33:327–338. http://dx.doi.org/10.4067/S0716-02082006000200006
Acosta Hospitaleche C, Reguero M (2010) First articulated skeleton of Palaeeudyptes gunnari from the late Eocene of Isla Marambio (Seymour Island), Antarctica. Antarct Sci 22:289–298. https://doi.org/10.1017/S0954102009990769
Acosta Hospitaleche C, Reguero M (2014) Palaeeudyptes klekowskii, the best-preserved penguin skeleton from the Eocene–Oligocene of Antarctica: Taxonomic and evolutionary remarks. Geobios 47:77–85. https://doi.org/10.1016/j.geobios.2014.03.003
Acosta Hospitaleche C, Tambussi C (2006) Skull morphometry of Pygoscelis (Sphenisciformes): inter and intraspecific variations. Polar Biol 29:728–734. https://doi.org/10.1007/s00300-006-0109-6
Ainley DG, Emison WB (1972) Sexual size dimorphism in Adélie pinguins. Ibis 114:267–271. https://doi.org/10.1111/j.1474-919X.1972.tb02613.x
Ainley DG, LeResche RE, Sladen WJL (1983) Breeding Biology of the Adélie Penguin. UC Press, Berkeley
Amprino R, Godina G (1947) La struttura della ossa nei vertebrati. Ricerche comparative negli anfibi e negli amnioti. Pont Acad Sci Comm 11:329–464
Bailleul AM, O’Connor J, Schweitzer MH (2019) Dinosaur paleohistology: review, trends and new avenues of investigation. PeerJ 7:e7764. https://doi.org/10.7717/peerj.7764
Bloom W, Bloom MA, McLean FC (1941) Calcification and ossification. Medullary bone changes in the reproductive cycle of female pigeons. Anat Rec 81:443–475. https://doi.org/10.1002/ar.1090810404
Bourdon E, Castanet J, de Ricqlès A, Scofield P, Tennyson A, Lamrous H, Cubo J (2009) Bone growth marks reveal protracted growth in New Zealand kiwi (Aves, Apterygidae). Biol Lett 5:639–642. https://doi.org/10.1098/rsbl.2009.0310
Canoville A, Schweitzer MH, Zanno LE (2019) Systemic distribution of medullary bone in the avian skeleton: ground truthing criteria for the identification of reproductive tissues in extinct Avemetatarsalia. BMC Evol Biol 19:1–20. https://doi.org/10.1186/s12862-019-1402-7
Canoville A, Chinsamy A, Angst D (2022) New Comparative Data on the Long Bone Microstructure of Large Extant and Extinct Flightless Birds. Diversity 14:1–30. https://doi.org/10.3390/d14040298
Castanet J. (2006). Time recording in bone microstructures of endothermic animals; functional relationships. CR Palevol 5:629–636. https://doi.org/10.1016/j.crpv.2005.10.006
Cerda IA, Tambussi CP, Degrange FJ (2015) Unexpected microanatomical variation among Eocene antarctic stem penguins (Aves: Sphenisciformes). Hist Biol 27:549–557. https://doi.org/10.1080/08912963.2014.896907
Chinsamy A (1995) Histological perspectives of growth in the birds Struthio camelus and Sagittarius serpentarius. Cour Forschinst Senckenb 181:317–323
Chinsamy A, Martin LD, Dodson P (1998) Bone microstructure of the diving Hesperornis and the volant Ichthyornis from the Niobrara Chalk of western Kansas. Cretaceous Res 19:225–235. https://doi.org/10.1006/cres.1997.0102
Chinsamy A, Raath MA (1992) Preparation of fossil bone for histological examination. Palaeontol Afr 29:39–44
Dacke CG, Arkle S, Cook DJ, Wormstone IM, Jones S, Zaidi M, Bascal ZA (1993) Medullary bone and avian calcium regulation. J Exp Biol 184:63–88. https://doi.org/10.1242/jeb.184.1.63
Emmerson L, Pike R, Southwell C (2011) Reproductive consequences of environment-driven variation in Adélie penguin breeding phenology. Mar Ecol Prog Ser 440:203–216. https://doi.org/10.3354/meps09265
Fattorini N, Olmastroni S (2021) Pitfalls and advances in morphometric sexing: insights from the Adélie penguin Pygoscelis adeliae. Polar Biol 44:1563–1573. https://doi.org/10.1007/s00300-021-02893-6
Forster, J. R. (1781). Historia aptenodytae. Generis avium orbi avstrali proprii. Commentat Soc Regiae Sci Gott 3:121–148
Garcia Marsà JA, Tambussi CP, Cerda IA (2020) First evidence of globuli ossei in bird (Aves, Spheniciformes). Implications on paleohistology and bird behaviour. Hist Biol 32:570–573. https://doi.org/10.1080/08912963.2018.1508288
Habib M (2010) The structural mechanics and evolutions of aquaflying birds. Biol J Linn Soc 99:687–690. https://doi.org/10.1111/j.1095-8312.2010.01372.x
Habib MB, Ruff CB (2008) The effects of locomotion on the structural characteristics of avian limb bones. Zool J Linn Soc 153:601–624. https://doi.org/10.1111/j.1096-3642.2008.00402.x
Hall BK (1991) What is bone growth? In: Sarnat BG, Dixon AD (eds) Fundamentals of Bone Growth. CRC Press, Boca Raton, pp 605–612
Hombron J, Jacquinot H (1841) Description de plusieurs oiseaux nouveaux ou peu connus, provenant de l’expédition autour du monde sur les corvettes L’Astrolabe et La Zélée. Ann Sci Nat Zool 2:312–320
Houde P (1987) Histological evidence for systematic position of Hesperornis (Odontornithes: Hesperornithiformes. Auk 104:125–129. https://doi.org/10.2307/4087243
Houssaye A (2009) “Pachyostosis” in aquatic amniotes: a review. Integr Zool 4:325–340. https://doi.org/10.1111/j.1749-4877.2009.00146.x
Houssaye A (2013) Palaeoecological and morphofunctional interpretation of bone mass increase: an example in Late Cretaceous shallow marine squamates. Biol Rev 88:117–139. https://doi.org/10.1111/j.1469-185X.2012.00243.x
Kerry KR, Agnew DJ, Clarke JR, Else GD (1992) Use of morphometric parameters for determination of sex in Adélie penguins. Wildl Res 19:657–664. https://doi.org/10.1071/WR9920657
Ksepka DT, Clarke JA, DeVries TJ, Urbina M (2008) Osteology of Icadyptes salasi, a giant penguin from the Eocene of Peru. J Anat 213:131–147. https://doi.org/10.1111/j.1469-7580.2008.00927.x
Ksepka DT, Werning S, Sclafani M, Boles ZM (2015) Bone histology in extant and fossil penguins (Aves: Sphenisciformes). J Anat 227:611–630. https://doi.org/10.1111/joa.12367
Jadwiszczak P, Acosta Hospitaleche C (2013) Distinguishing between two Antarctic species of Eocene Palaeeudyptes penguins: a statistical approach using tarsometatarsi. Pol Polar Res 34:237–252. https://doi.org/10.2478/popore-2013-0020
Jennings S, Varsani A, Dugger KM, Ballard G, Ainley DG (2016) Sex-based differences in Adélie penguin (Pygoscelis adeliae) chick growth rates and diet. PLoS One 11:e0149090. https://doi.org/10.1371/journal.pone.0149090
de Margerie E, Robin JP, Verrier D, Cubo J, Groscolas R, Castanet J. (2004). Assessing a relationship between bone microstructure and growth rate: a fluorescent labeling study in the king penguin chick (Aptenodytes patagonicus). J Exp Biol 207:869–879. https://doi.org/10.1242/jeb.00841
Martínez I (1992) Order Sphenisciformes. In: del Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the world Volume 1 Ostrich to Ducks. Lynx Edicions, Bellaterra, pp 140–160
Meister W (1962) Histological Structure of the Long Bones of Penguins. Anat Rec 143:377–387. https://doi.org/10.1002/ar.1091430408
Padian K, de Ricqlès A, Horner JR (2001) Dinosaurian growth rates and bird origins. Nature 412:405–408. https://doi.org/10.1038/35086500
Padian K, Woodward HN (2021) Archosauromorpha: Avemetatarsalia – Dinosaurs and Their Relatives. In: de Buffrénil V, de Ricqlès AJ, Zylberberg L, Padian K (eds) Vertebrate Skeletal Histology and Paleohistology. CRC Press, Boca Raton, pp 511–549
Polito MJ, Clucas GV, Hart T, Trivelpiece WZ (2012) A simplified method of determining the sex of Pygoscelis penguins using bill measurements. Mar Ornithol 40:89–94
Raikow RJ, Bicanovsky L, Bledsoe AH (1988) Forelimb joint mobility and the evolution of wing-propelled diving in birds. Auk 105:446–451
de Ricqlès A, de Buffrenil V (2001) Bone histology, heterochronies and the return of tetrapods to life in water: where are we? In: Mazin JM, de Buffrenil V (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. Friedrich Pfeil, Munich pp 289–310
Simpson GG (1972) Pliocene penguins from North Canterbury, New Zealand. Rec of the Canterb Mus 9:159–182
Simpson GG (1976) Penguins: Past and Present, Here and There. Yale University Press, London
Scolaro JA, Stanganelli ZB, Gallelli H, Vergani DF (1991) Sexing of adult Adélie penguins by discriminant analysis of morphometric measurements. CCAMLR Sci 1990:543–550
Stonehouse B (1975) The Biology of Penguins. University Park Press, Maryland
Trathan PN, Ballard G (2015) Género Pygoscelis. In: Garcia Borboroglu P, Dee Boersma P (eds) Pingüinos, historia natural y conservación. Vazquez Mazzini Editores, Buenos Aires, pp 39–94
Turvey ST, Green OR, Holdaway RN (2005) Cortical growth marks reveal extended juvenile development in New Zealand moa. Nature 435:940–943. https://doi.org/10.1038/nature03635
Tütken T, Pfretzschner HU, Vennemann TW, Sun G, Wang YD (2004) Paleobiology and skeletochronology of Jurassic dinosaurs: implications from the histology and oxygen isotope compositions of bones. Palaeogeogr Palaeoclimatol Palaeoecol 206:217–238. https://doi.org/10.1016/j.palaeo.2004.01.005
Wagler JG (1832) Isis, oder Encyclopaedische Zeitung 25. Editing Pygoscelis, 281
Walsh SA, Suárez ME (2006) New penguin remains from the Pliocene of Northern Chile. Hist Biol 18:119–130. https://doi.org/10.1080/08912960600640796
Wilson LE, Chin K (2014) Comparative osteohistology of Hesperornis with reference to pygoscelid penguins: the effects of climate and behaviour on avian bone microstructure. R Soc Open Sci 1:1–16. https://doi.org/10.1098/rsos.140245
Winkler DW, Billerman SM, Lovette IJ (2020) Penguins (Spheniscidae), version 1.0. In: Billerman SM, Keeney BK, Rodewald PG, Schulenberg TS (eds) Birds of the World. Cornell Lab of Ornithology, Ithaca. https://doi.org/10.2173/bow.spheni1.01

No competing interests reported.

Download PDF

Journal Publication

published 18 Jul, 2023

Read the published version in Polar Biology →

Editorial decision: Major revision
15 Jun, 2023
Reviewers agreed at journal
05 Mar, 2023
Reviews received at journal
27 Feb, 2023
Reviewers agreed at journal
27 Feb, 2023
Reviewers invited by journal
27 Feb, 2023
Editor assigned by journal
27 Feb, 2023
Submission checks completed at journal
24 Feb, 2023
First submitted to journal
23 Feb, 2023

You are reading this latest preprint version

Osteohistological variations in the Antarctic penguin Pygoscelis adeliae (Aves, Sphenisciformes)

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Materials And Methods

Results

Microanatomy

Histology

Discussion

Sex differences

Outer circumferential layer in Pygocelis adeliae

Vascular patterns

Conclusions

Declarations

References

Additional Declarations

Status:

Journal Publication

Version 1