MORE EGGS THE BETTER: EGG FORMATION IN CAPTIVE BARN OWLS (TYTO ALBA)
Durant, Joel M
ABSTRACT.-We studied rapid yolk deposition (RYD) in Barn Owls (Tyto alba) on the basis of the analysis of 26 eggs laid by “dye-dosed” captive female Barn Owls in five different broods. Pictures of yolks were examined to assess daily rates of yolk deposition. We used those data in combination with data from the dissection of ovaries of another five breeding females. We found that the total duration between initiation of RYD and laying of the corresponding egg was only 13.6 days, with an interval between yolk completion and oviposition of 2.4 days. The total number of follicles that may have given eggs was found to be 25. That high number of follicles and the short RYD period explain the particularly high reproductive potential of this nocturnal raptor species. Received 22 January 2003, accepted 15 September 2003.
RESUME.-Nous avons etudie le depot rapide du vitellus (DRV) chez Tyto alba. L’etude est basee sur l’analyse de 26 oeufs repartis en cinq couvees provenant de femelles de Tyto alba captives ayant ingere des pigments lipophiles. Les photographies de vitellus ont ete examinees pour estimer les taux journaliers de depot en vitellus. Nous avons exploite ces donnees combinees a d’autres issues de la dissection des ovaires de cinq autres femelles reproductrices. Nous avons trouve que la duree totale entre l’initiation du DRV et l’eclosion des oeufs correspondant etait seulement de 13,6 jours, avec un intervalle de 2,4 jours entre l’achevement de la formation du vitellus et l’oviposition. Un total de 25 follicules se seraient developpes pour donner des oeufs. Ce grand nombre de follicules et la courte duree de la periode de DRV expliquent le potentiel reproductif important de ce rapace nocturne.
REPRODUCTION EFFORT PER breeding attempt is one of the main parameters defining life-history strategies (Stearns 1992). In birds, the yolk constitutes the major energy content of an egg (Sutherland and Rahn 1987). An estimate of the daily amount of yolk deposited on developing ova and the sequence of laying are important when evaluating the total cost of egg production. In birds, the vast majority of the yolk mass is deposited in a relatively short period of time compared to other oviparous vertebrates; in some passerines, rapid yolk deposition (RYD) may last only three days per yolk (Ricklefs 1974, Grau 1984). During RYD, growing follicles take up from the blood the yolk precursors that are produced and secreted by the liver (Griffin and Hermier 1988, Shen et al. 1993); follicle growth occurs in a hierarchy with at most one follicle reaching maturity and being ovulated each day (Christians and Williams 2001).
Clearly, the energy cost of egg production is determined by clutch size and the variation in rate of growth of follicles recruited, duration of the follicles’ growth, or both. Even though the energetic demands during clutch formation were modelled 30 years ago (King 1973), and a technique is available to assess daily energy-nutrient demands during yolk formation (Warren and Conrad 1939, Gilbert 1972, Grau 1976), few studies have attempted to empirically examine such demands in birds (Astheimer and Grau 1985).
In birds that lay big clutches, total number of eggs in formation (Haywood 1993) and laying interval (Astheimer 1985) must be taken into account to estimate the daily yolk-deposition rate. Moreover, the number of follicles that undergo yolk deposition commonly exceeds number of eggs actually laid (Meijer et al. 1989), which suggests that unlaid yolks become atretic (Erpino 1973, Gilbert et al. 1983). Thus, it is important to take into account the actual number of eggs laid, all eggs resorbed before oviposition, and all the follicles that undergo atresia, when assessing the energy-nutrient requirements for an entire reproductive attempt.
Among raptors, the Barn Owl (Tyto alba) has an exceptionally high reproductive potential, which is rather similar to that of passerine birds. This owl species commonly lays clutches of four to seven eggs (Taylor 1994), where clutch size varies widely according to food availability (Mikkola 1983, Taylor 1994). No accurate data are available on the laying interval, ovary structure, and timing of yolk development in Barn Owls. We predicted that the high reproductive potential in this altricial species, associated with a low daily energy requirement of egg synthesis (Durant et al. 2000, Vezina and Williams 2002), is due to a long RYD period and a possibility of recruiting a larger number of follicles for RYD than eggs actually laid.
The aim of our study was to characterize the phases and timing of egg formation in captive Barn Owls to understand the high potentiality of laying in this species. Likewise, we also conducted an ovary analysis and determined the number of developing follicles.
The study was performed on captive European Barn Owls that were part of a breeding program conducted since 1985 in our laboratory. Each pair of owls was housed separately in an outside aviary (5 × 4 × 2.5 m) where a nest box was available. They were fed daily with laboratory mice (Mus musculus). Laying takes place from March to October. The average egg laying interval was 2.4 ± 0.5 days (n = 96) (i.e. laying occurred at different times of the day for successive eggs).
DETERMINATION OF RAPID YOLK DEPOSITION
Rapid yolk deposition is the deposition period for lipoprotein yolk on the enlarging proteinaceous primordial follicle. A lipophilic dye, Sudan black B, was given orally and used as a date marker of the yolk structure during follicle development (see Warren and Conrad 1939, Gilbert 1972, Grau 1976 for techniques). Because the yolk is laid down in layers by addition of material to the outer margin (Gilbert 1979), the dye ingestion results in a distinct ring within the yolk, the deposition of that ring can be linked to the date of dye ingestion.
The experiment was conducted on five captive female Barn Owls. The average clutch size was 5.0 ± 0.4 eggs with a total of 26 eggs. Nests were checked daily to see when the laying started. just after the laying of their first egg, females were fed with a gelatin capsule containing 50 mg of dye and weighed. Birds were thereafter dye fed every second day until the last egg was laid. To minimize disturbance of breeding birds, the gelatin capsule was put under the skin of a freshly killed mouse (see Close et al. 1997 for procedure for small mammals). In the morning, the mouse was substituted for the prey store created by the male during the previous night inside the nest box. In the afternoon, we checked that the mouse was eaten and then put the prey store back into the nest. The average delay between deposition of the mouse with the capsule in nest and its disappearance (i.e. its ingestion by the female) was 6.6 h (0-10.5 h).
Freshly laid eggs (n = 26) were collected for dyering analysis and replaced immediately with dummy eggs to prevent a possible prolongation of laying (Haywood 1993). Eggs were measured (length and breadth) with a caliper to the nearest 1.0 mm, weighed to the nearest 0.01 g, and frozen at -15°C. Frozen eggs were treated later following Grau (1976, 1996). They were put into hot water (40°C) for a few seconds, shell and membranes removed, and frozen contents fixed in 4% formalin at 60°C for 16 h. Shells were dried at 60°C for 48 h and weighed.
After fixation, all albumen was removed; spherical yolks were weighed, cut in half, and one half stained with 6% potassium dichromate for 16 h at 60°C.
Enlarged slides were used to measure yolk radius, to locate the position of the dyed yolk rings, and to measure the relative thickness of each yolk layer delimited by dye. The slides allowed us to estimate the daily yolk-growth increment (Astheimer and Grau 1990) and to calculate the duration of RYD.
Yolk deposition in birds follows a more-or-less exponential curve (see Astheimer and Grau 1990 for a review). To compare the RYD rate with an ANCOVA (Zar 1984), we fitted a linear equation after log-transformation of the y-axis (yolk-deposition rate) to each egg data-set with more than three dye rings (n = 9). Among the five clutches, only one had several eggs (n = 4) with more than three dye rings. That clutch was used to analyze the potential effect of the laying order on RYD rate.
Ovaries of five other breeding females obtained from another study (Durant et al. 2000) were used. Fresh ovaries were weighed and dissected under a binocular microscope. Five follicle types were distinguished (Lofts and Murton 1973): (1) RYD follicles undergoing rapid yolk development; (2) primordial follicles, which are small follicles not yet recruited into a follicular hierarchy of RYD; (3) mature follicles; (4) postovulatory follicles, which are those ruptured after ovulation (remnant of a follicle whose ovum was ovulated); and (5) atretic follicles, which are the follicles that undergo atresia before ovulation. To eliminate confusion between atretic and postovulatory follicles, those follicles were excised from the ovary and cut in half for examination of their internal structures. A postovulatory follicle appears as a flat yellow purse attached to the ovary by a large isthmus. On the other hand, depending on the stage of atresia, the cut atretic follicle has a dense zone surrounding the visible oocyte containing a yolky residue or is occluded. In a more advance stage, an atretic follicle is easily distinguished without examination of its internal structure by its deformed or shrunken appearance.
DETERMINATION OF RAPID YOLK DEPOSITION
The yolks (n = 26) measure on average 18.8 ± 0.1 mm (SE) for an average mass of 3.4 ± 0.1 g (SE). Calculated average yolk density was 0.96 ± 0.01 cm^sup 3^ (SE).
Because we started feeding dye to birds after the laying of the first egg, that first egg was not used in the analysis of RYD. The second-laid egg of all clutches studied did not show dye rings, which meant that the yolk deposition was completed for those eggs at the time of dye ingestion (i.e. laying of the first egg). Consequently, the first egg marked with a dye ring was always the third-laid egg. Each following egg had thereafter one more dye ring than the preceding one.
The more peripheral dye ring observed in a yolk (i.e. the most recently deposited dye ring) corresponds to ingestion of pigment 2.4 days before laying. The time period between the end of RYD and oviposition is then >2.4 days. The smaller and most central dye ring observed (i.e. deposited nearest to the initiation of RYD) corresponds to pigment ingestion 13.6 days before laying (fifth dye ring). Thus, the RYD period lasts 11.2 days.
We calculated the mass of the sphere delimited by each dye ring assuming that the yolk is homogeneous and applying its density. Cumulative yolk mass expressed as a function of time is presented in Figure 1. The smallest dye-ring diameter observed (3.7 mm) corresponded to 20% of the final yolk diameter and weighed 0.03 g. The yolk enlargement rate was on average 1.6 mm day^sup -1^.
Neither the laying order nor the different clutches had an effect on the RYD (ANCOVA: F = 0.76, df = 6 and 9, P > 0.25; and F = 2.38, df = 6 and 21, respectively). Consequently, we pooled data from the different eggs and broods and fitted to them a second-order equation (Fig. 1) that indicates that RYD started and stopped 13.2 and 2.5 days, respectively, before laying.
Using values for beginning and ending of RYD, a timing of events could be drawn (Fig. 2).
OVARY AND OVIDUCT ANALYSIS
The ovary structure presented numerous follicles at different stages of development (Table Y). Follicles with a mass
Each postovulatory follicle corresponded to an ovulated ovum; the smallest (i.e. oldest), visible postovulatory follicle corresponded to an egg laid eight days before killing (the third of a five-egg clutch, sacrifice taking place three days after the last laying).
Each ovary presented several atretic follicles. We assumed that atretic follicles >0.03 g came from RYD follicles that had failed to develop further. Only those atretic follicles could have given an egg and were considered (Table 1).
RATE OF YOLK DEPOSITION
This is the first time that the RYD duration has been determined for Barn Owls and to our knowledge only the second time for a raptor species (Meijer et al. 1989). We determined that RYD in Barn Owls starts 13.6 days before laying and lasts ~11 days. Barn Owls are known to be able to lay replacement clutches, second and third clutch (Taylor 1994). In the aviary, we observed that the first egg of the replacement clutch could be laid as early as 14 days (n = 21) after the clutch removal. That value is consistent with the time necessary to produce an egg, from follicle recruitment to oviposition, and indicates that the Barn Owl needs only 14 days to produce a second clutch.
Is RYD affected by the birds’ captivity? To our knowledge, no study addresses that problem. Obviously, a difference in diet could affect RYD. However, the body mass increase of captive and wild females during the prelaying period is similar in duration and intensity (Durant 2000). In our study, all birds were fed ad libitum. Such ad libitum feeding of the female during egg synthesis is not uncommon in the wild. Indeed, the male often provides its nest-confined mate an excess of prey, which accumulates in the nest room (Taylor 1994, Durant et al. 1996, Durant 2000). The main prey of the European Barn Owl during reproduction in eastern France is the common vole (Microtus arvalis, Muller 1991), which has a higher average caloric value than, but a similar composition as, the laboratory mice fed to our birds (7.74 and 6.6 kJ g^sup -1^, respectively; Wijnandts 1984, Durant et al. 2000). Thus, it seems safe to assume that the diet provided in the present study mimics the natural conditions and that the RYD measured is representative of the RYD in the field, or at least faster.
The Barn Owl RYD period has long been compared to other altricial species (studied in the wild and in captivity). For example, Rock Pigeons (Columbia livia), which lay eggs of similar mass (18 g), exhibit an RYD of 5-8 days (Carey et al. 1980, Sotherland and Rahn 1987), whereas Eurasian Kestrels (Falco tinnunculus) have an RYD of only 9 days for eggs of 20 g (Meijer et al. 1989). Shags (Phalacrocorax aristocelis), another altricial species, have an RYD of 13.5 days, similar to Barn Owls, for eggs weighing >40 g (Grau 1996). In Barn Owls, the yolk mass/RYD duration ratio is only 0.3 in comparison to the average yolk mass/RYD ratio of 1.9 (0.1-9.0) for altricial birds with eggs of various masses (1.6-330 g; calculated from values for 10 species from Carey et al. 1980, Walsberg 1983, Sotherland and Rahn 1987, Astheimer and Grau 1990, Grau 1996). Barn Owls seem to have a slower yolk-deposition rate than might be expected considering its egg size. In addition, the energy content of Barn Owl eggs is lower than that for other altricial species (Durant et al. 2000). As a consequence of those two factors, Barn Owls have a lower daily nutritional requirement per egg with two expected advantages. First, with a low daily deposition cost per yolk, females can deposit simultaneously relatively more yolk in follicles, within the energy constraint of food intake. Interestingly, laying order does not seem to have any effect on the yolk growth rate in Barn Owls, indicating that competition between follicles for nutrients is small. The deposition of several eggs at the same time is a phenomenon already described for other birds (sec below). second, it could be advantageous if food supply is limiting in terms of energy or specific nutrients because the daily requirement is smaller.
In Barn Owls, it was shown that the nutrients required for egg formation could be obtained by routine food intake in that species (Durant et al. 2000). That relatively low daily nutritional requirement is accentuated if we look at mass relationship between egg and female (Walsberg 1983, Carey 1996). That relationship predicts that Barn Owls should lay eggs weighing 25.5 g instead of the 17.5 g found here (using the equation for cavity-nesting birds; log egg mass = log 0.61 + 0.631 log female body mass; Taylor 1994). As a consequence, such small eggs may allow Barn Owls to lay large clutches. However, laying small and numerous eggs could be a disadvantage if a longer posthatching development period results in a higher prédation rate for nestlings (Halupka 1998). Barn Owls, like other cavity-nesting species, are more secure from predation (Martin and Li 1992).
OVULATION AND FOLLICLE SELECTION
In our study, we showed that Barn Owls produced more follicles than eggs laid (Table 1) as has been already observed in other bird species (Haywood 1993). However, an original result is that ovaries presented several atretic follicles at the completion of the clutch. That indicated that there was an ovum present ready to be ovulated when the last egg was laid. Indeed, the removal of eggs as soon as they are laid induces prolongation of laying, that is, egg development (stopped after the laying of 18 eggs; Y. Handrich pers. obs.). Thus, surplus yolks may allow Barn Owls to lay new eggs without an increase in the laying interval. Barn Owl eggs hatch asynchronously because of a start of incubation at the first laying. An increased laying interval would create a large hatching interval for last-born chicks with potential negative effects on their survival (Durant and Handrich 1998, Durant 2002).
Barn Owls seem to be indeterminate layers (Haywood 1993), birds that have great flexibility in the number of eggs they can lay. In this species, the fact that the ovary produces on average of 25 follicles during the laying period certainly adds to that flexibility. In the field, Barn Owls also show great plasticity in number of eggs laid, with clutch sizes from 2 to 18 eggs (Taylor 1994) in response to variations in prey abundance (Mikkola 1983, Taylor 1994).
We thank C. Fritsch for help in laboratory analysis, and G. H. Visser, J. Reynolds, T. J. Seller, D. A. Nelson, K. G. Smith, and two anonymous referees for helpful comments on an earlier draft of the manuscript. We also thank J. Kent and D. Gremillet for editing help. The experiments were done in compliance with current French laws and after program acceptance by French authorities: Authorisation of the Ministere de l’Agriculture et de la Peche n° 04196.
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Associate Editor: D. A. Nelson
JOEL M. DURANT,1 SYLVIE MASSEMIN, AND YVES HANDRICH
Centre d’Ecologie et Physiologie Energetiques, Centre National de la Recherche Scientifique, 23 rue Becquerel, F-67087 Strasbourg Cedex 02, France
1 Present address: Centre for Ecological and Evolutionary Synthesis, Division of Zoology, Department of Biology, University of Oslo, P.O. Box 1050 Blindem, 0316 Oslo, Norway. E-mail: firstname.lastname@example.org
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