- Email: [email protected]
Preferred natural food of breeding Kakapo is a high value source of calcium and vitamin D
G Model SBMB 4552 No. of Pages 3
Journal of Steroid Biochemistry & Molecular Biology xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Journal of Steroid Biochemistry & Molecular Biology journal homepage: www.elsevier.com/locate/jsbmb
Review
Preferred natural food of breeding Kakapo is a high value source of calcium and vitamin D P.R. von Hursta,* , R.J. Moorhouseb , D. Raubenheimerc a
Institute of Food Science and Technology, School of Food and Nutrition, College of Health, Massey University, Private Bag 102904, Auckland, New Zealand Department of Conservation, 653 Wairoa Gorge Road, RD1 Brightwater, Nelson 7091, New Zealand c Charles Perkins Centre, Faculty of Veterinary Science, School of Biological Sciences, Level 4 East, D17—Education and Research Hub, The Charles Perkins Centre, The University of Sydney, NSW 2006, Australia b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 17 June 2015 Received in revised form 28 September 2015 Accepted 19 October 2015 Available online xxx
The Kakapo, a large NZ native parrot, is under severe threat of extinction. Kakapo breed only in years when the local podocarps, including rimu (Dacrydium cupressinum), are fruiting heavily, and the fruit are the preferred food both in the diet of breeding females and for provisioning chicks. Attempts to provide a supplementary food during years of poor fruit supply have failed to encourage breeding. Nutrient analysis of rimu berries reveals high calcium content (8.4 mg/g dry matter) which would be essential for both egg shell production and the growing skeleton of the chick. Vitamin D is also critical for these processes and for the maintenance of calcium homeostasis, but the source of vitamin D for these nocturnal, ground-dwelling vegetarians is unknown. Objective: To examine the vitamin D status of adult Kakapo, and to investigate the possibility that rimu berries provide vitamin D as well as calcium, thus differentiating them from the supplementary foods provided to date. Method: Previously collected and frozen serum from 10 adult birds (6 females, 4 males) was assayed for 25(OH)D3 and D2. Two batches of previously frozen rimu berries were analysed for vitamin D3 and D2. Results: Vitamin D status of the 10 adult birds was very low; mean 4.9 nmol/l, range 1–14 nmol/l 25(OH) D3. No 25(OH)D2 was detected in any of the birds. High levels of D2 and moderate levels of D3 were found in the rimu berries. Conclusion: Traditionally it has been considered that the D3 isoform of this endogenously produced secosteroid is produced only in animals. However, D3 has been reported in the leaves of plants of the Solanacae family (tomato, potato, capsicum). The avian vitamin D receptor (VDR) is thought to have a much greater affinity for the D3 form. Therefore if rimu fruit are able to provide breeding Kakapo with D3, and are a plentiful source of calcium, they could be the perfect food package for breeding and nesting birds. Of wider importance, this finding challenges conventional understanding that D3 production is exclusive to animals, and that there are no high concentration food sources of vitamin D. ã 2015 Published by Elsevier Ltd.
Keywords: Vitamin D Parrots Kakapo
Contents 1. 2. 3. 4. 5.
Introduction . . . . Method . . . . . . . . Results . . . . . . . . Discussion . . . . . . Conclusion . . . . . Source of funding References . . . . .
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* Corresponding author. E-mail addresses: [email protected] (P.R. von Hurst), [email protected] (R.J. Moorhouse), [email protected] (D. Raubenheimer). http://dx.doi.org/10.1016/j.jsbmb.2015.10.017 0960-0760/ ã 2015 Published by Elsevier Ltd.
Please cite this article in press as: P.R. von Hurst, et al., Preferred natural food of breeding Kakapo is a high value source of calcium and vitamin D, J. Steroid Biochem. Mol. Biol. (2015), http://dx.doi.org/10.1016/j.jsbmb.2015.10.017
00 00 00 00 00 00 00
G Model SBMB 4552 No. of Pages 3
2
P.R. von Hurst et al. / Journal of Steroid Biochemistry & Molecular Biology xxx (2015) xxx–xxx Table 2 Vitamin D content of frozen rimu berries.
1. Introduction The large New Zealand native parrot, the Kakapo, is under threat of extinction. The birds breed only in years when the native rimu (Dacrydium cupressinum) are fruiting heavily, with the fruit being the preferred food both for breeding females and for provisioning chicks [1]. Breeding females forage on rimu trees, and will even climb the 25 m tall trunks to collect up to 500–600 g of ripe fruit for each chick daily [1]. Nutrient analysis of rimu berries reveals high calcium content which would be essential for both egg shell production and the growing skeleton of the chick. The ripe berries also provide protein and fatty acids (Table 1) as well as a range of both digestible and non-digestible carbohydrates [1]. The provision of substitute foods mimicking calcium content of rimu berries [2] has had an ambivalent result in the promotion or support of breeding in seasons when the rimu crop was small, or the berries failed to ripen on the trees. The role of vitamin D in egg development has been well characterised in laying hens [3]. The content of the vitamin D receptor (VDR) in the egg shell gland (ESG) increases markedly on maturation in the laying hen, and vitamin D appears to have an active role in maintaining functionality of the ESG [3]. Laying performance and egg shell stability are significantly influenced by dietary vitamin D intake, as are the concentrations of both vitamin D and 25(OH)D in the egg yolk [4]. Vitamin D is also critical for the maintenance of calcium homeostasis and is associated with bone strength in the growing bird [5]. Although much of the knowledge about the importance of vitamin D in birds comes from laying hens, its role in the breeding cycle of the kakapo can be assumed to be just as important. However, the source of vitamin D for these nocturnal, ground-dwelling vegetarians is unknown. Therefore this small study aimed to investigate the vitamin D content of rimu berries, and the vitamin D status of non-breeding birds. 2. Method Stored samples of both kakapo serum and previously collected rimu berries were analysed as follows: Previously collected and frozen serum from 10 adult birds (6 females, 4 males) was assayed by Canterbury Health Laboratory using LC–MS/MS for 25(OH)D3 and D2. None of the birds tested were breeding at the time. Two batches of rimu berries, previously collected by Department of Conservation staff from two different locations and stored at 80 C, were analysed by the Massey University Nutrition Laboratory for vitamin D3 and D2 AOAC. Official Methods: 982.29, modified (isocratic reversed-phase high performance liquid chromatography). 3. Results Vitamin D status of the 10 adult birds was very low; mean serum 25(OH)D3 4.9 nmol/l, range 1–14 nmol/l. No 25(OH)D2 was detected in any of the birds.
Table 1 Nutrient analysis of ripe rimu berries [1]. Macronutrient distribution
Protein Lipids Carbohydrate
Micronutrient content (mg/g dry matter)
7.23% Calcium 10.90% Potassium 77.69% Phosphorous
Entire fruit
Seed
8.42 3.68 1.11
10.22 3.16 1.67
Calcium content compares very favourably with almonds (2.5 mg/g) and sesame seeds (1.3 mg/g), both considered to be ‘good’ sources of calcium.
Rimu fruit
Vitamin D2
Vitamin D3
Batch 1—mg/100 g (IU/100 g) Batch 2—mg/100 g (IU/100 g) Mean
73 (2920) 67 (2680) 70 (2800)
18 (720) 5 (200) 11.5 (460)
High levels of D2 and moderate levels of D3 were found in the rimu berries (Table 2). 4. Discussion This study was initiated by the search for a suitable food to replace or complement the rimu berry in the years of poor crops, and encourage breeding. Raubenheimer and Simpson [6] used geometric models to show that the natural breeding foods of remaining kakapo, rimu berries, have very high ratios of calcium to macronutrients, and proposed that calcium limitation might explain why supplementary feeds have not succeeded in triggering reproduction. However, a source vitamin D is necessary to utilise dietary calcium, giving rise to the question of how vitamin D requirements are met for this forest-dwelling, nocturnal, flightless bird, which has minimal sun exposure. We hypothesised that there must be a dietary source, especially at times of greatest need such as breeding and feeding nestlings. Given that rimu berries are not just preferred, but almost exclusive, feed during these times, it seemed possible that they may contain some vitamin D. The findings, however, were unexpected as not only were there very high concentrations of vitamin D2 found in the berries, but moderate amounts of D3 were found as well. Traditionally it has been considered that vitamin D3 or cholecalciferol is the isoform produced in animals and D2 (ergocalciferol) is the plant form of this endogenously produced secosteroid. However, D3 has been reported in the leaves of plants of the Solanacae family (tomato, potato, capsicum) [7], supporting the current findings. It is estimated that growing chicks consume approximately 550 g of rimu fruit per day [1]. Therefore, given our analysis of their primary food source, they receive on average 450 mg or 17,930 IU total vitamin D (385 mg or 15,400 IU D2 and 63 mg or 2530 IU D3) along with 4620 mg of calcium, per day. This would appear to be more than sufficient to support growth to the adult mass of approximately 1.5 kg, and helps explain the importance of this food source to the breeding success of the kakapo. Avian vitamin D binding protein is shown to have a much greater affinity for the D3 isoform, during various stages of metabolism, than D2, with the latter also having a much higher clearance rate [8]. Consequently, vitamin D3 is the more active form, possibly by as much as ten times [8]. Therefore if rimu fruit are able to provide breeding Kakapo with vitamin D3 as well as very high levels of D2, and are a plentiful source of calcium, they would be the perfect food package for breeding and nesting birds. From the beginning of the breeding season in spring, the females consume a diet very high in rimu berries which at that time are unripe. The berries tested in this study were gathered in March and April, and were mostly ripe fruit. The vitamin D content of the unripe berries is unknown at this stage and invites further investigation. There has been much speculation on the form of potential ‘triggers’ for nesting in the female bird, as this does seem to be linked to the fruiting of the rimu. Harper et al. speculated that as the rimu fruit “provides no significant nutrients other than energy”, the female kakapo had either a cognitive or hormonal response to crop size, mating only if the green crop predicted an abundant crop of ripe fruit on which to feed their chicks [9].
Please cite this article in press as: P.R. von Hurst, et al., Preferred natural food of breeding Kakapo is a high value source of calcium and vitamin D, J. Steroid Biochem. Mol. Biol. (2015), http://dx.doi.org/10.1016/j.jsbmb.2015.10.017
G Model SBMB 4552 No. of Pages 3
P.R. von Hurst et al. / Journal of Steroid Biochemistry & Molecular Biology xxx (2015) xxx–xxx
We hypothesise that there may be an hormonal response due to increasing vitamin D status as the female consumes the early fruit. Vitamin D deficiency has been shown to negatively impact fertility in both humans [10] and murine models [11], and as mentioned above, the egg shell gland in laying hens has been shown to be responsive to vitamin D status [3]. Unfortunately, it was not possible at the time of this small study to acquire serum from chicks or breeding females, but we assume that in comparison to the very low levels in the adult birds tested, their vitamin D status must be considerably greater. The next step in this intriguing investigation will include measuring adult birds during breeding, growing chicks, and rimu fruit throughout the ripening process. 5. Conclusion These findings offer a possible explanation for the failure of supplemental foods to satisfactorily encourage breeding when rimu berries are in short supply, and a clue towards development of a nutritionally complete alternative. Of wider importance, this finding challenges conventional understanding that there are no naturally high concentration food sources of vitamin D, and provides further evidence that D3 production is not exclusive to animals.
3
References [1] Y. Cottam, D. Merton, W. Hendriks, Nutrient composition of the diet of parentraised kakapo nestlings, Notornis 53 (2006) 90–99. [2] G. Elliot, D. Merton, P. Jansen, Intensive management of a critically endanged species: the kakapo, Biol. Conserv. 99 (1) (2001) 121–133. [3] A. Bar, Calcium homeostasis and vitamin D metabolism and expression in strongly calcifying laying birds, Comp. Biochem. Physiol. A 151 (2008) 477–490. [4] J. Lietzow, H. Kluge, C. Brandsch, N. Seeburg, F. Hirche, M. Glomb, et al., Effect of short-term UVB exposure on vitamin D concentration of eggs and vitamin D status of laying hens, J. Agric. Food Chem. 60 (2012) 799–804. [5] P. Mattila, J. Valaja, L. Rossow, E. Venalainen, T. Tupasela, Effect of vitamin D2 and D3 entriched diets on egg vitamin D content, production and bird condition during an entire production period, Poulty Sci. 83 (2004) 433–440. [6] D. Raubenheimer, S. Simpson, The challenge of supplementary feeding: can geometric analysis help save the kakapo? Notornis 53 (2006) 100–111. [7] R. Jäpelt, D. Silvestro, J. Smedsgaard, P. Jensen, J. Jakobsen, Quantification of vitamin D3 and its hydroxylated metabolites in waxy leaf nightshade (Solanum glaucophyllum Desf.), tomato (Solanum lycopersicum L.) and bell pepper (Capsicum annuum L.), Food Chem. 138 (2013) 1206–1211. [8] D. Hoy, C. Ramberg, R. Horst, Evidence that discrimination against ergocalciferol by the chick is the result of enhanced metabolic clearance rates for its nomo- and dihydroxylated metabolites, J. Nutr. 118 (1988) p633–p638. [9] G. Harper, G. Elliott, D. Eason, R. Moorhouse, What triggers nesting of kakapo (Strigops habroptilus)? Notornis 53 (2006) 160–163. [10] M. Irani, Z. Merhi, Role of vitamin D in ovarian physiology and its implication in reproduction: a systematic review, Fertil. Steril. 102 (2) (2014) . [11] E. Lerchbaum, B. Obermayer-Pietsch, Vitamin D and fertility: a systematic reveiw, Eur. J. Endrocrinol. 166 (5) (2012) 765–778.
Source of funding Massey University.
Please cite this article in press as: P.R. von Hurst, et al., Preferred natural food of breeding Kakapo is a high value source of calcium and vitamin D, J. Steroid Biochem. Mol. Biol. (2015), http://dx.doi.org/10.1016/j.jsbmb.2015.10.017
Journal of Steroid Biochemistry & Molecular Biology xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Journal of Steroid Biochemistry & Molecular Biology journal homepage: www.elsevier.com/locate/jsbmb
Review
Preferred natural food of breeding Kakapo is a high value source of calcium and vitamin D P.R. von Hursta,* , R.J. Moorhouseb , D. Raubenheimerc a
Institute of Food Science and Technology, School of Food and Nutrition, College of Health, Massey University, Private Bag 102904, Auckland, New Zealand Department of Conservation, 653 Wairoa Gorge Road, RD1 Brightwater, Nelson 7091, New Zealand c Charles Perkins Centre, Faculty of Veterinary Science, School of Biological Sciences, Level 4 East, D17—Education and Research Hub, The Charles Perkins Centre, The University of Sydney, NSW 2006, Australia b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 17 June 2015 Received in revised form 28 September 2015 Accepted 19 October 2015 Available online xxx
The Kakapo, a large NZ native parrot, is under severe threat of extinction. Kakapo breed only in years when the local podocarps, including rimu (Dacrydium cupressinum), are fruiting heavily, and the fruit are the preferred food both in the diet of breeding females and for provisioning chicks. Attempts to provide a supplementary food during years of poor fruit supply have failed to encourage breeding. Nutrient analysis of rimu berries reveals high calcium content (8.4 mg/g dry matter) which would be essential for both egg shell production and the growing skeleton of the chick. Vitamin D is also critical for these processes and for the maintenance of calcium homeostasis, but the source of vitamin D for these nocturnal, ground-dwelling vegetarians is unknown. Objective: To examine the vitamin D status of adult Kakapo, and to investigate the possibility that rimu berries provide vitamin D as well as calcium, thus differentiating them from the supplementary foods provided to date. Method: Previously collected and frozen serum from 10 adult birds (6 females, 4 males) was assayed for 25(OH)D3 and D2. Two batches of previously frozen rimu berries were analysed for vitamin D3 and D2. Results: Vitamin D status of the 10 adult birds was very low; mean 4.9 nmol/l, range 1–14 nmol/l 25(OH) D3. No 25(OH)D2 was detected in any of the birds. High levels of D2 and moderate levels of D3 were found in the rimu berries. Conclusion: Traditionally it has been considered that the D3 isoform of this endogenously produced secosteroid is produced only in animals. However, D3 has been reported in the leaves of plants of the Solanacae family (tomato, potato, capsicum). The avian vitamin D receptor (VDR) is thought to have a much greater affinity for the D3 form. Therefore if rimu fruit are able to provide breeding Kakapo with D3, and are a plentiful source of calcium, they could be the perfect food package for breeding and nesting birds. Of wider importance, this finding challenges conventional understanding that D3 production is exclusive to animals, and that there are no high concentration food sources of vitamin D. ã 2015 Published by Elsevier Ltd.
Keywords: Vitamin D Parrots Kakapo
Contents 1. 2. 3. 4. 5.
Introduction . . . . Method . . . . . . . . Results . . . . . . . . Discussion . . . . . . Conclusion . . . . . Source of funding References . . . . .
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* Corresponding author. E-mail addresses: [email protected] (P.R. von Hurst), [email protected] (R.J. Moorhouse), [email protected] (D. Raubenheimer). http://dx.doi.org/10.1016/j.jsbmb.2015.10.017 0960-0760/ ã 2015 Published by Elsevier Ltd.
Please cite this article in press as: P.R. von Hurst, et al., Preferred natural food of breeding Kakapo is a high value source of calcium and vitamin D, J. Steroid Biochem. Mol. Biol. (2015), http://dx.doi.org/10.1016/j.jsbmb.2015.10.017
00 00 00 00 00 00 00
G Model SBMB 4552 No. of Pages 3
2
P.R. von Hurst et al. / Journal of Steroid Biochemistry & Molecular Biology xxx (2015) xxx–xxx Table 2 Vitamin D content of frozen rimu berries.
1. Introduction The large New Zealand native parrot, the Kakapo, is under threat of extinction. The birds breed only in years when the native rimu (Dacrydium cupressinum) are fruiting heavily, with the fruit being the preferred food both for breeding females and for provisioning chicks [1]. Breeding females forage on rimu trees, and will even climb the 25 m tall trunks to collect up to 500–600 g of ripe fruit for each chick daily [1]. Nutrient analysis of rimu berries reveals high calcium content which would be essential for both egg shell production and the growing skeleton of the chick. The ripe berries also provide protein and fatty acids (Table 1) as well as a range of both digestible and non-digestible carbohydrates [1]. The provision of substitute foods mimicking calcium content of rimu berries [2] has had an ambivalent result in the promotion or support of breeding in seasons when the rimu crop was small, or the berries failed to ripen on the trees. The role of vitamin D in egg development has been well characterised in laying hens [3]. The content of the vitamin D receptor (VDR) in the egg shell gland (ESG) increases markedly on maturation in the laying hen, and vitamin D appears to have an active role in maintaining functionality of the ESG [3]. Laying performance and egg shell stability are significantly influenced by dietary vitamin D intake, as are the concentrations of both vitamin D and 25(OH)D in the egg yolk [4]. Vitamin D is also critical for the maintenance of calcium homeostasis and is associated with bone strength in the growing bird [5]. Although much of the knowledge about the importance of vitamin D in birds comes from laying hens, its role in the breeding cycle of the kakapo can be assumed to be just as important. However, the source of vitamin D for these nocturnal, ground-dwelling vegetarians is unknown. Therefore this small study aimed to investigate the vitamin D content of rimu berries, and the vitamin D status of non-breeding birds. 2. Method Stored samples of both kakapo serum and previously collected rimu berries were analysed as follows: Previously collected and frozen serum from 10 adult birds (6 females, 4 males) was assayed by Canterbury Health Laboratory using LC–MS/MS for 25(OH)D3 and D2. None of the birds tested were breeding at the time. Two batches of rimu berries, previously collected by Department of Conservation staff from two different locations and stored at 80 C, were analysed by the Massey University Nutrition Laboratory for vitamin D3 and D2 AOAC. Official Methods: 982.29, modified (isocratic reversed-phase high performance liquid chromatography). 3. Results Vitamin D status of the 10 adult birds was very low; mean serum 25(OH)D3 4.9 nmol/l, range 1–14 nmol/l. No 25(OH)D2 was detected in any of the birds.
Table 1 Nutrient analysis of ripe rimu berries [1]. Macronutrient distribution
Protein Lipids Carbohydrate
Micronutrient content (mg/g dry matter)
7.23% Calcium 10.90% Potassium 77.69% Phosphorous
Entire fruit
Seed
8.42 3.68 1.11
10.22 3.16 1.67
Calcium content compares very favourably with almonds (2.5 mg/g) and sesame seeds (1.3 mg/g), both considered to be ‘good’ sources of calcium.
Rimu fruit
Vitamin D2
Vitamin D3
Batch 1—mg/100 g (IU/100 g) Batch 2—mg/100 g (IU/100 g) Mean
73 (2920) 67 (2680) 70 (2800)
18 (720) 5 (200) 11.5 (460)
High levels of D2 and moderate levels of D3 were found in the rimu berries (Table 2). 4. Discussion This study was initiated by the search for a suitable food to replace or complement the rimu berry in the years of poor crops, and encourage breeding. Raubenheimer and Simpson [6] used geometric models to show that the natural breeding foods of remaining kakapo, rimu berries, have very high ratios of calcium to macronutrients, and proposed that calcium limitation might explain why supplementary feeds have not succeeded in triggering reproduction. However, a source vitamin D is necessary to utilise dietary calcium, giving rise to the question of how vitamin D requirements are met for this forest-dwelling, nocturnal, flightless bird, which has minimal sun exposure. We hypothesised that there must be a dietary source, especially at times of greatest need such as breeding and feeding nestlings. Given that rimu berries are not just preferred, but almost exclusive, feed during these times, it seemed possible that they may contain some vitamin D. The findings, however, were unexpected as not only were there very high concentrations of vitamin D2 found in the berries, but moderate amounts of D3 were found as well. Traditionally it has been considered that vitamin D3 or cholecalciferol is the isoform produced in animals and D2 (ergocalciferol) is the plant form of this endogenously produced secosteroid. However, D3 has been reported in the leaves of plants of the Solanacae family (tomato, potato, capsicum) [7], supporting the current findings. It is estimated that growing chicks consume approximately 550 g of rimu fruit per day [1]. Therefore, given our analysis of their primary food source, they receive on average 450 mg or 17,930 IU total vitamin D (385 mg or 15,400 IU D2 and 63 mg or 2530 IU D3) along with 4620 mg of calcium, per day. This would appear to be more than sufficient to support growth to the adult mass of approximately 1.5 kg, and helps explain the importance of this food source to the breeding success of the kakapo. Avian vitamin D binding protein is shown to have a much greater affinity for the D3 isoform, during various stages of metabolism, than D2, with the latter also having a much higher clearance rate [8]. Consequently, vitamin D3 is the more active form, possibly by as much as ten times [8]. Therefore if rimu fruit are able to provide breeding Kakapo with vitamin D3 as well as very high levels of D2, and are a plentiful source of calcium, they would be the perfect food package for breeding and nesting birds. From the beginning of the breeding season in spring, the females consume a diet very high in rimu berries which at that time are unripe. The berries tested in this study were gathered in March and April, and were mostly ripe fruit. The vitamin D content of the unripe berries is unknown at this stage and invites further investigation. There has been much speculation on the form of potential ‘triggers’ for nesting in the female bird, as this does seem to be linked to the fruiting of the rimu. Harper et al. speculated that as the rimu fruit “provides no significant nutrients other than energy”, the female kakapo had either a cognitive or hormonal response to crop size, mating only if the green crop predicted an abundant crop of ripe fruit on which to feed their chicks [9].
Please cite this article in press as: P.R. von Hurst, et al., Preferred natural food of breeding Kakapo is a high value source of calcium and vitamin D, J. Steroid Biochem. Mol. Biol. (2015), http://dx.doi.org/10.1016/j.jsbmb.2015.10.017
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We hypothesise that there may be an hormonal response due to increasing vitamin D status as the female consumes the early fruit. Vitamin D deficiency has been shown to negatively impact fertility in both humans [10] and murine models [11], and as mentioned above, the egg shell gland in laying hens has been shown to be responsive to vitamin D status [3]. Unfortunately, it was not possible at the time of this small study to acquire serum from chicks or breeding females, but we assume that in comparison to the very low levels in the adult birds tested, their vitamin D status must be considerably greater. The next step in this intriguing investigation will include measuring adult birds during breeding, growing chicks, and rimu fruit throughout the ripening process. 5. Conclusion These findings offer a possible explanation for the failure of supplemental foods to satisfactorily encourage breeding when rimu berries are in short supply, and a clue towards development of a nutritionally complete alternative. Of wider importance, this finding challenges conventional understanding that there are no naturally high concentration food sources of vitamin D, and provides further evidence that D3 production is not exclusive to animals.
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References [1] Y. Cottam, D. Merton, W. Hendriks, Nutrient composition of the diet of parentraised kakapo nestlings, Notornis 53 (2006) 90–99. [2] G. Elliot, D. Merton, P. Jansen, Intensive management of a critically endanged species: the kakapo, Biol. Conserv. 99 (1) (2001) 121–133. [3] A. Bar, Calcium homeostasis and vitamin D metabolism and expression in strongly calcifying laying birds, Comp. Biochem. Physiol. A 151 (2008) 477–490. [4] J. Lietzow, H. Kluge, C. Brandsch, N. Seeburg, F. Hirche, M. Glomb, et al., Effect of short-term UVB exposure on vitamin D concentration of eggs and vitamin D status of laying hens, J. Agric. Food Chem. 60 (2012) 799–804. [5] P. Mattila, J. Valaja, L. Rossow, E. Venalainen, T. Tupasela, Effect of vitamin D2 and D3 entriched diets on egg vitamin D content, production and bird condition during an entire production period, Poulty Sci. 83 (2004) 433–440. [6] D. Raubenheimer, S. Simpson, The challenge of supplementary feeding: can geometric analysis help save the kakapo? Notornis 53 (2006) 100–111. [7] R. Jäpelt, D. Silvestro, J. Smedsgaard, P. Jensen, J. Jakobsen, Quantification of vitamin D3 and its hydroxylated metabolites in waxy leaf nightshade (Solanum glaucophyllum Desf.), tomato (Solanum lycopersicum L.) and bell pepper (Capsicum annuum L.), Food Chem. 138 (2013) 1206–1211. [8] D. Hoy, C. Ramberg, R. Horst, Evidence that discrimination against ergocalciferol by the chick is the result of enhanced metabolic clearance rates for its nomo- and dihydroxylated metabolites, J. Nutr. 118 (1988) p633–p638. [9] G. Harper, G. Elliott, D. Eason, R. Moorhouse, What triggers nesting of kakapo (Strigops habroptilus)? Notornis 53 (2006) 160–163. [10] M. Irani, Z. Merhi, Role of vitamin D in ovarian physiology and its implication in reproduction: a systematic review, Fertil. Steril. 102 (2) (2014) . [11] E. Lerchbaum, B. Obermayer-Pietsch, Vitamin D and fertility: a systematic reveiw, Eur. J. Endrocrinol. 166 (5) (2012) 765–778.
Source of funding Massey University.
Please cite this article in press as: P.R. von Hurst, et al., Preferred natural food of breeding Kakapo is a high value source of calcium and vitamin D, J. Steroid Biochem. Mol. Biol. (2015), http://dx.doi.org/10.1016/j.jsbmb.2015.10.017