Revista Brasileira de Zootecnia © 2011 Sociedade Brasileira de Zootecnia ISSN 1806-9290 www.sbz.org.br
R. Bras. Zootec., v.40, p.60-67, 2011 (supl. especial)
Relationship among the economically important ratites: a clustering approach based on their reproductive biology Théa Mirian Medeiros Machado1, Irek Artur Malecki2, Graeme Bruce Martin2 1 2
UFV Departamento de Zootecnia, Campus da Universidade Federal de Viçosa, MG, Brasil, UWA Institute of Agriculture (Animal Production), The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
ABSTRACT - The African ostrich, Australian emu and South American greater rhea have been chosen for this study because they are all farmed for meat, leather, oil, feathers, eggs and eggshell. A comparison of the three species is interesting for both academic discussion and management practice. They are classified as ratites based on their non-carinate sternum and lack of breast muscles, a group for which the phylogenetic relationships are still not completely clear. Our purpose in this paper is to compare reproductive biology of the farmed ratites based on observations in the literature for: the effects of photoperiod and rainfall on reproduction, sexual and parental behaviour, sexual dimorphism, spermatozoa characteristics, eggshell colour and body weight/competition for mates between gender. Each of these features was coded as present or absent and the data were then subjected to cluster analysis using the Jaccard Coefficient, the Matrix Distance and the Unweighted Pair Group Method with Arithmetic Mean. The outputs show that ostrich cluster with rhea while emu is on a different branch of the phenogram. The unroot tree showed three branches for the three species, with the emu at the terminal of the longer branch. Rhea and ostrich diverge with respect to sexual dimorphism, mating system and male parental care. This last character is in common between rhea and emu. Based on these results, the Australian ratite differs from the American and African ratites. Key Words: breeding season, egg, parental care, reproductive behaviour, sexual dimorphism, spermatozoa
Relação entre ratitas de importância econômica: uma abordagem de agrupamento baseada em suas características reprodutivas RESUMO - A avestruz Africana, o emu australiano e a ema sul-americana foram escolhidos para este estudo porque são criados comercialmente para produção de carne, pele, óleo, plumas e ovos, cujas cascas são ainda aproveitadas. A comparação entre as três espécies é de interesse tanto acadêmico quanto para práticas de manejo. Elas são classificadas como ratitas com base em seu esterno não-carinado e na ausência de músculos peitorais, um grupo cujas relações filogenéticas ainda não foram completamente elucidadas. Nosso propósito neste artigo é comparar a biologia reprodutiva destas ratitas de interesse zootécnico, com base na literatura, quanto a: efeito do fotoperíodo e das precipitações sobre a reprodução, comportamentos sexual e parental, dimorfismo sexual, características do espermatozóide, cor da casca do ovo e peso corporal/competição para acasalamento entre gêneros. Cada uma destas características foi codificada para presença e ausência e os dados foram submetidos à análise de agrupamento com o emprego do coeficiente de Jaccard, da matriz de distâncias, e do método das médias nãoponderadas. O resultado mostra que avestruz agrupa com ema enquanto emu é um braço distinto do fenograma. A árvore sem raiz mostra três ramos para as três espécies, com o emu na extremidade do ramo mais longo. Ema e avestruz divergem quanto a dimorfismo sexual, sistema de acasalamento e cuidados parentais. Este último caráter é comum entre ema e emu. Com base nestes resultados, as ratitas australianas diferem das americanas e das africanas. Palavras-chave:
estação reprodutiva, comportamento reprodutivo, cuidados parentais, dimorfismo sexual, espermatozóide, ovo
Introduction Modern birds were long ago divided taxonomically into Neognathae and Palaeognathae on the basis of the characteristics of their palates (Huxley, 1867). The Palaeognathae includes ratites and the tinamous, for which the phylogenetic relationship is still incompletely elucidated Corresponding author:
[email protected]
(Cracraft, 1974; Cooper et al., 1992; Lee et al., 1997; Härlid & Arnason, 1999; van Tuinen & Hedges, 2001; Haddrath & Baker, 2001; Waters & Craw, 2006; Hackettet al., 2008). The ratites include two South American birds, the greater rhea (Rhea america) and the lesser rhea (Pterocnemia pennata), the Australian emu (Dromaius novaehollandiae), the Australian and New Guinean
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cassowary (Casuarius spp.), the New Zealand kiwi (Apteryx spp) and the African ostrich (Struthio camelus). Among extinct ratites are the New Zealand moas (Dinornis sp.), the Madagascan elephant bird (Aepyornis sp.) and the New Caledonian Sylvornis (Carrer & Kornfeld, 1999). With exception of the kiwi, they have heavily muscled legs for running and defence, a noncarinate sternum and lack of breast muscles, and the retention of chick-like feathers into adulthood, a phenomenon termed ‘neoteny’, that is apparently driven by thyroid hormones (Dawson, 1996; Blache et al., 2001). Karyotypically, birds have a conserved sexchromosome system, with a ZW constitution in the females. In the neognaths, the W is smaller than the Z and rich in Cbanding material whereas, in all ratite birds, the Z and W chromosomes differ little in size and are poor in C+ heterochromatin content (Pigozzi & Solari, 1999). The karyotypes and sex chromosomes of palaeognathous birds are highly conserved on both morphological and molecular levels (Nishida-Umehara et al., 2007). The diploid number of
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chromosomes is 80 for the ostrich and 82 for rhea and emus with some differences in the position of the centromeres (Takagi et al., 1972). The phylogenetic relationships proposed for the ratites (Figure 1) vary greatly with the taxa set, the markers and the statistical method used for clustering (Lee et al., 1997). According to Cracraft (1974), Rheidae cluster with Struthionidae whereas Dromiceidae cluster with Casuaridae. Kilnner (2006) founded a similar result working with Apterygidae instead Dromiceidae. According to van Tuinen et al. (1998) and van Tuinen & Hedges (2001), the ostrich is phylogenetically basal and the rheas cluster with Australasian ratites. However, according Cooper et al. (1992) and Grellet-Tinner (2006), the oldest of the actual ratites is the Rhea. These last authors also differentiate the Australasian ratites from those of Africa and South America. Taylor et al. (1999) compared the ratites using six highly polymorphic microsatellite loci from the emu and found that the rhea had diverged most from the emu, followed by the ostrich and then the kiwi.
Figure 1 - Ratite evolutionary clusters according to different markers and data setsA) Cracraft (1974) and Lee et al. (1997) from morphology data; B) van Tuinen et al. (1998) from mitochondrial rRNA and tRNA genes; C) Cooper et al. (1992) from rRNA sequences (presented here as a simplified scheme) and Lee et al. (1997) from mitochondrial rRNA, COI, COII, cytochrome b, and tRNA genes; D) van Tuinen & Hedges (2001) from mtRNA, DNA-DNA hybridization, and transferrin immunological distances; E) Kilnner (2006) from clutch variation; F) Grellet-Tinner (2006) from egg and eggshells with inclusion of fossil taxa in the analysis. R. Bras. Zootec., v.40, p.60-67, 2011 (supl. especial)
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Relationship among the economically important ratites: a clustering approach based on their reproductive biology
The combination of long evolutionary (Handford & Mares, 1985) and the geographical separation (Waters & Craw, 2006) with the common neotenous development (Dawson, 1996; Härlid & Arnason, 1999) suggest fundamental similarities in the biology of the ratite species, thus leading to interesting comparisons. Our purpose in this paper is to focus on reproductive biology among the ostrich, emu and greater rhea. These species have been chosen because they are all farmed for a variety of products, including meat, leather, oil, feathers, eggs and eggshell (Martin, 1999; Malecki et al., 2001; Al-Nasser et al., 2003; Howarth et al., 2008; Hoffman, 2008; Carrer & Kornfeld, 1999; Silva, 2001).
Material and Methods The clustering of ostrich, emu and rhea was based on features described in the literature. Each feature was coded as 1 (present) or zero (absent). The Jaccard Coefficient and the Matrix Distance were calculated. A phenogram and an unroot tree in the Philip format were produced using the Unweighted Pair Group Method with Arithmetic Mean by DendroUPGMA (Garcia-Vallvé & Puigbo, 2009). The only features considered for clustering were those that showed variation among species: the effects of photoperiod and rainfall on reproduction, sexual and parental behaviour, sexual dimorphism, body weight and competition for mates between genders, spermatozoa characteristics and eggshell colour. Photoperiod and rainfall Birds show pronounced seasonal breeding at all latitudes, and many are able to predict and prepare for a forthcoming breeding opportunity, there by maximizing reproductive potential (Sharp, 1996). In general, the circannual rhythm in reproduction is cued to the annual cycle of changes in daylength, but this relationship is not absolute – species from high latitudes need a longer daylength to start egg laying than those from low latitudes; similarly, highland species require a longer photoperiod to initiate breeding than lowland birds. The breeding season of desert species is often related to the daylength cycle but it is also sensitive to the ecological consequences of water storage. Other species are opportunist and have the capacity to remain close to breeding condition for a long period (Murton & Westwood, 1977). Finally, decreasing daylength initiates breeding in most species, but increasing daylength is stimulatory in others, with the final outcome dependent on a combination of photostimulation and photorefractoriness (Sharp & Blache, 2003).
Machado & Rocha (2006) tested photoperiodism in the greater rhea by subjecting 2½-year-old birds to three increasing day lengths in a 600m2 aviary shed at 21°S in Brazil from April to June. Each group comprised 2 males and 5 females and was placed in a box illuminated by six 20W fluorescent lamps. The first group was exposed to natural daylength (about 10h30min) and the others were placed under artificial long days: 13.5h (05:15-18:45) or 16.5h (03:4520:15). The daylength was increased from natural to treatment length over six days, after which data were collected for egg-laying and broody behaviour for 10 weeks. In the first group, no eggs were laid. In the 13.5 h group, egglaying began two weeks after the data collection started and 50 eggs were produced. In the 16.5 h group, the egg-laying began the day after data collection started and 66 eggs were laid and one of the two males began showing broody behaviour. The rhea was thus confirmed as a long-day breeder in which clutch size responds positively to hours of light per day. The reproductive responses of birds to variations in daylength usually depend on direct intracranial light perception rather than indirect perception by the eyes, as is the case in mammals. This means that skin and feather colour of the cranium can play a role in seasonal breeding patterns. Saveur (1996) reported in the sparrow that artificially darkening the cranium blocks the sexual response to long days whereas Ali & Cheng (1985) found that genetically blind hens produced more eggs per bird day compared to sighted control hens. The issue of feather colour might be relevant to the seasonal breeding patters of the rhea. The greater rhea was initially classified by geographic distribution and feather colour. From north-east Brazil to south of Paraná, Rhea americana americana (Linné, 1758) is grey or grayish brown and usually has a dark crown, nape, base of the neck and upper back. In the southeast of the state of Mato Grosso, south of Bolivia, Paraguay and Argentina, Rhea americana albescens (Arribalzaga & Holmberg, 1878) is white. In the south of Brazil, Rhea americana intermedia (Rothschield & Chubb, 1914) is an intermediary colour (Dani, 1993). This raises a few questions. Is the colour of the greater rhea a factor in its reproductive strategy? Do they need to become lighter to be more photosensitive at the high latitudes? Does the greater rhea read light by the cranial pathway? Rocha (2008) answered this last question with Rhea americana americana kept indoors. When the birds were expressing reproductive behaviour (wing display, calls, swollen neck, copulation, nest ceremony and egglaying), Rocha (2008) painted their crown with nankeen black ink. In both sexes, painting the heads led to a complete R. Bras. Zootec., v.40, p.60-67, 2011 (supl. especial)
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loss of all signs of reproductive activity within only a few days, in contrast to the unpainted rheas. Therefore, in this ratite species at least, the reproductive response to photoperiod depends on direct intracranial light perception, as in non-ratite birds. The ostrich is considered photoperiod-dependent, with the breeding season being induced by an increase in daylength (Degen et al., 1994; Hicks-Alldredge, 1998), although this is not an absolute seasonality because they can breed all year round (Hicks, 1992; Degen et al., 1994). In farmed ostriches in eastern Australia, the egg-laying season is May to December (from early winter to early summer), but there is rarely an absence of eggs laid in any month (More, 1996). Reproduction in farmed ostrich also seems to be linked to feed intake so it is concentrated in the rainy season (Degen et al., 1994). However, in wild African ostrich, breeding is mostly seen in the dry season, with hatching before the beginning of heavy rainfall (Ullrey & Allen, 1996). The ostrich settle on an area to place their nest, usually remote from watering holes and other potential sources of disturbance (Handford & Mares, 1985). In Brazil, a rain-bearing front can interrupt egg laying (Carrer & Kornfeld, 1999). In young birds, the maturation of the ovary and the testis is affected by nutrition as well as daylength (Madekurozwa, 2002a, b). The number and weight of eggs laid per female also increases with age (Ipek & Sahan, 2004). Emus in Australia are also seasonal breeders with the egg-laying season beginning in April-May and ending in August-September, thus being focused on the winter months (Malecki & Martin, 2002). Eggs are almost never laid outside this period, consistent with this ratite being a strict short-day breeder (Sharp & Blache, 2003). However, it appears that rainfall advances the onset of egg-laying in semi-arid regions where rainfall events are unpredictable, and extends the laying season (thus leading to production of more eggs) in the Mediterranean region where the rainfall pattern is more consistent between years. In both study sites, nutrition was ad libitum, so these observations suggest that we need to question the dominance of the role of photoperiod in timing the onset and termination of the breeding season of the emu (Williams et al., 1997; Martin, 1999). Male emus have been studied in detail in southwestern Australia by Malecki et al. (1998). They found that plasma concentrations of luteinizing hormone (LH) and testosterone are higher during autumn-winter than during spring-summer, whereas prolactin concentrations begin to rise around the winter solstice and peak near the spring equinox. Testicular mass and testicular concentrations of testosterone were
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higher in the breeding than in the non-breeding season, although variations were observed among individuals and months. The seminiferous tubules had a larger diameter in the breeding season. Rhea distribution excludes humid forests and ranges from 5oS to 41 oS (Handford & Mares, 1985). Brazil ranges from 5°N to 33°S and reproduction is not seasonal in the north but quite seasonal in the south for many species. The breeding season of the greater rhea in Brazil occupies the whole year in the northeast (Dani, 1993) but only the spring in the southeast and south (Silva, 2001). According Góes et al. (2010), captive greater rhea in São Paulo breed from MayJuly to October-November and testosterone levels differ between the breeding (53 ± 18 ng/ml) and the non-breeding season (5.6 ± 3.8 ng/ml). The seasonal distribution of breeding activity thus seems to be related more to latitude than to the feed provided by the rainy season. The rainfall is more evenly distributed in the south than in southeast and, in the hinterland of the northeast it is very seasonal with low total annual precipitation. In Argentina, rainfall could have affect nest desertion directly as a consequence of flooding, or indirectly as a consequence of nest predation. In years of high rainfall, male rhea nest in the hither areas where armadillos, one of the predators, are more abundant. Nest success had no correlation with rainfall but tended to increase as the reproductive season progress. Late breeders could have more success than early breeders because they have more fat reserves and was less prone to nest desertion (Fernandez & Reboreda, 1998). Sexual behaviour and parental care In the wild, ostrich breeding groups include one adult male per 3-4 females. The territorial male selects the nest site and then begins building the nest. Only one female, the ‘major’ female, accepts the site, guards and shares, about 42 days, incubation of her own eggs plus those laid by ‘minor’ females with the territorial male. Major female lays 5-11 eggs and can incubate about 20 eggs, with the surplus being pushed 1"2 m away from the nest to perish. The major female avoids pushing out her own eggs. ‘Major’ females may also act as ‘minor’ females in the nests of other territorial males. However, in small populations, monogamous breeding units appear to predominate (Bertram, 1979; Handford & Mares, 1985; Ullrey & Allen, 1996; Kimwele & Graves, 2003). According Handford & Mares (1985), the Australasian ratites appear largely monogamous and are much less gregarious than ostriches and rheas. Despite reasonably strong pair-bonding, female emus engage in sequential R. Bras. Zootec., v.40, p.60-67, 2011 (supl. especial)
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polyandry after their primary male partner sits on the nest and will even return to the nest or lay eggs fertilized by another male (Coddington & Cockburn, 1995; Taylor et al., 2000; Blache et al., 2005). An emu nest may contain eggs from more than one female (Taylor et al., 2000). The hen lays from five to twenty eggs and the male bird incubates the eggs usually for 56 to 60 days (Eastman, 1969). The rhea is polygamous. Each male displays for many females, composes and defends his harem and builds a single polygynous nest. The females display sequential polyandry, consorting with a new reproductively active male when the most recent dominant male becomes more interested in his nest than in harem defense. The number of eggs per female per season is 10-40 (Sick, 1985; Dani, 1993). Only the male rhea incubates the eggs, for 37-38 days, and takes care of the offspring (Handford & Mares, 1985; Dani, 1993; Codenotti et al., 1995). The phylogenetic basal position of Paleognathes birds is used to support the hypothesis for the male-only parental care to be the original breeding system of living birds (Varricchio et al., 1997; Prum, 2008). Male emus have exclusive parental care, and incubate the eggs without getting up or eating or drinking (Buttemer & Dawson, 1989). Greater rhea males also have exclusive parental care – they build the nest, rarely abandon the nest to feed, and also feed and defend the chicks, for 4-6 months after hatching (Raikow, 1969; Codenotti & Alvarez, 2001; Fernandes & Rebodera, 1998, 2003). Male ostriches generally incubate at night while one of the hens, usually the ‘major’ hen, incubates during the day (Handford & Mares, 1985; Blache et al., 2005). Sexual dimorphism, body weight and gender competition for mates Only the ostrich, among the ratites, shows marked sexual dimorphism. The males are larger and black and white, while females are smaller and greyish-brown colour (Handford & Mares, 1985; Davies, 2002). Female ostriches appear to come into breeding before the males and both sexes display a repertoire of reproductive behaviour (Davies,
2002). Female emus are on average larger than males and are often observed in mated pairs (Davies, 2002). Female emus assume the dominant role in courtship and fight vigorously among themselves for access to unpaired males (Coddington & Cockburn, 1995). Male greater rheas are larger than females and dominate the competition for mates (CluttonBrock & Vincent, 1991; Codenotti & Alvarez, 2001; Davies, 2002). All male ratites have an intromittent organ (phallus), and the female ostrich and emu have a diminutive organ (Fowler, 1991). Spermatozoa characteristics and eggshell colour The spermatozoa of the ratite birds are characterized by: a conical acrosome surrounding the nucleus; a fibrous sheath around most of the axoneme; and an elongated distal centriole occupying the entire midpiece. Dromaius is distinctly different from the Struthio and Rhea which are closely related to one another by the presence of a rod-like endonuclear perforatorium (Baccetti et al., 1991). The egg shell of the rhea and the ostrich is ivory when the eggs are newly laid, later fading to white or cream (Bertram & Burger, 1981; Davies, 2002). By contrast, the emu eggshell is granulated and coloured, with variations from light green to black-green during incubation (Eastman, 1969). Wallace (1889) hypothesized that “that the primitive colour of birds’ eggs was white, a colour that prevails now among the other egg-bearing vertebrates - lizards, crocodiles, turtles, and snakes; and we might, therefore, expect that this colour would continue where its presence had no disadvantages”. This hypothesis was reviewed by Kilner (2006) and contested by Igic et al. (2010). Egg colour could have co-evolved with interspecific brood parasitism (laying eggs for a host) (Wallace, 1890; Takasu, 1998, 2003) and sexual selection (Moreno & Osorno, 2003; Soler et al., 2005). According to Collins (1993), village weavers (Ploceus cucullatus) have two autosomal loci for eggshell colour, each locus with a pairs of recessive/dominant alleles and their combinations result in turquoise, white or emeraldturquoise eggs. Chickens have also two autosomal loci
Table 1 - Major features of the reproductive biology of the economically important ratites Ostrich Spermatozoa with a rod-like endonuclear perforatorium Exclusive male parental care Breeding season in the increasing daylength Ivory, white or cream eggshells Absolutely polygamous and weak pair-bonding in the wild Egg-laying and hatching decrease with heavy rainfall Marked sexual dimorphism Females are larger than males and compete for mates
Emu
X X X X X X
Rhea X X X X X X
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affecting eggshell colour (Wei et al., 1992). The genetic origin of the ratite eggshell colour has not been established and we can only speculate about the effects of mating system and the environment that have led to the green eggshell of the emu.
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Conclusions Based on reproductive features ostrich, rhea and emu, the Australian emu differs significantly from the American rheas and African ostrich, with the rhea and ostrich showing considerable similarity.
Results and Discussion Acknowledgements Some major features of the reproductive biology or ostrich, rhea and emu are summarized in Table 1. The Matrix Distance based on the Jaccard coefficient (Table 2), the phenogram (Figure 2A) and the unroot tree (Figure 2B) show quantitatively and graphically that there is more similarity between ostrich and rhea than between each them and the emu. These results agree with the findings of Cracraft (1974), Lee et al. (1997), Kilnner (2006) and Grellet-Tinner (2006) using different variables. The divergent characters between ostrich and rhea are sexual dimorphism, mating system and parental care. This last character is in common between rhea and emu.
Table 2 - Matrix distance based on Jaccard coefficient for reproductive features of ratites
Ostrich Emu Rhea
Ostrich
Emu
Rhea
0
1.000 0
0.429 0.857 0
A
B
Figure 2 - Phenogram (A) and unroot tree (B) for the ostrich, emu and rhea, based on reproductive features, employing Jaccard coefficient and UPGMA algorithm.
This study was supported by Capes, as visiting scholar grant at the University of Western Australia.
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Relationship among the economically important ratites: a clustering approach based on their reproductive biology
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