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Umbilical scarring in hatchling American alligators
Aquaculture 239 (2004) 155 – 159 www.elsevier.com/locate/aqua-online
Umbilical scarring in hatchling American alligators J.J. Wiebe a,*, M.S. Sepu´lveda b, J.E. Buckland b, S.R. Anderson c, T.S. Gross a,b a
USGS-Florida Integrated Science Center, Center for Aquatic Resource Studies, 7920 N.W. 71st Street, Gainesville, FL 32653, USA b Department of Physiological Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32611, USA c Cypress Creek Farm, Starke, FL 32091, USA Received 23 January 2004; received in revised form 22 March 2004; accepted 24 March 2004 Available online
Abstract Umbilical scarring is the presence of excess scar tissue deposited between abdominal dermal layers at the site of yolk sac absorption in hatchling American alligators (Alligator mississippiensis). The presence of this dermal condition plays a key evaluatory role in the overall quality and subsequent value for various commercial leather products. Despite the prevalent nature of this condition, currently the industry has no standardized protocols for its quantification. The objectives of this study were to examine the relationship between hatchling weight and age and incidence of umbilical scarring and to develop a quantifiable and reproducible technique to measure this dermal condition in hatchling American alligators. Thirty eggs from each of nine clutches were incubated in two separate incubators at different facilities and hatchling umbilical scarring was measured at 2 and 10 days of age using digital calipers. Umbilical area was calculated by multiplying umbilical length times umbilical width. There was a significant effect of both age and clutch on umbilical area (overall decline of 64%) by 10 days post-hatch. However, only five of the nine clutches utilized expressed a noticeable decline in the size of this dermal condition (range 67 – 74%). We had hypothesized that larger hatchlings would have larger umbilical areas and a slower rate of improvement in this condition during the first few days post-hatch. The differences in umbilical area and percent decline with age across clutches, however, were not associated with differences in initial hatchling weights. Within clutches and time periods, hatchling weight had no significant effect on the size and/or rate of decline of this condition. D 2004 Published by Elsevier B.V. Keywords: Umbilical scarring; American alligator hatchlings; Egg quality; Leather goods
* Corresponding author. Tel.: +352-378-8181x400; fax: +352-395-6608. E-mail address: [email protected] (J.J. Wiebe). 0044-8486/$ - see front matter D 2004 Published by Elsevier B.V. doi:10.1016/j.aquaculture.2004.03.027
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1. Introduction In hatchling American alligators (Alligator mississippiensis), umbilical scarring can be defined as the presence of excess scar tissue deposited between abdominal dermal layers at the site of yolk sac absorption. In Florida, licensed alligator farming operations have an estimated 5– 25% incidence of umbilical scarring leading to annual financial losses of approximately US$650,000 (Anderson, unpublished data). Currently, however, there are no standardized protocols available to quantify this dermal condition. Research on alligator production showed eggs at a temperature range of 31.5 –31.7 jC produces hatchlings that grow at an accelerated rate and reduces the incidence of animal hunting (Joanen et al., 1987). At the point of hatching, a hatchling should have absorbed the majority (>95%) of the egg yolk constituents as well as closed the abdominal dermal layer surrounding the yolk sac (Ferguson, 1985). However, accelerated embryonic growth based on incubation temperature may be one of the primary causative agents for the incidence of umbilical scarring and other developmental abnormalities (Deeming and Ferguson, 1991). Differences in alligator embryonic and hatchling growth, however, could also be related to factors other than incubation temperature. Data from our laboratory and others would suggest that, within sites, growth rates can vary significantly across clutches (Webb et al., 1992, Wiebe et al., unpublished data). Among a variety of potential factors, these clutch differences could be the result of genetic influences and/or variations in maternal and subsequent egg nutritional qualities. The objective of the current study was to examine the relationship between hatchling weight and age and incidence of umbilical scarring in the American alligator. We hypothesized that umbilical scarring would be positively related to alligator hatchling weight and that the size of this dermal condition during the first 10 days post-hatch would decrease at a faster rate in leaner animals. An additional objective was to develop a quantifiable and reproducible technique to measure this condition in hatchling American alligators.
2. Materials and methods In order to test the effect of hatchling weight on umbilical scarring, nine clutches collected from a single site in central Florida were utilized due to expected clutch variability on hatchling weight. Thirty eggs from each clutch were divided into equal size (n = 15 eggs/incubation site) and incubated as clutch specific replicates in two different facilities: FISC Florida Integrated Science Center (FISC) and Cypress Creek Farm (CCF) at similar temperature and humidity conditions (31.5 F 1 jC and 95 F 5%, respectively). Eggs were randomized between the two facilities in part to lesson the effect of clutch on future analyses (Fig. 1) (Webb et al., 1992). Eggs were incubated in plastic pans (48 36 16.5 cm) using sphagnum moss as the substrate. Incubation substrate was hydrated at least once a week until hatching. Eggs were left to hatch on their own to limit potential artificial trauma to the umbilical region. Hatch rates were calculated as (number of hatchlings/total number of eggs incubated, Table 1). At 2 days post-hatch, hatchlings
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Fig. 1. Photographic illustration of umbilical scarring at day 2.
were weighed (g), and umbilical scarring was evaluated by measuring umbilical length (distance between the anterior and posterior regions of the umbilical opening) and umbilical width (measured at the median portion of the umbilical region) (Fig. 1). Umbilical area (mm2) was calculated by multiplying umbilical length umbilical width. Umbilical measurements were collected using digital calipers (Mitotoyo, Japan). In addition, a digital photograph was taken of the minimum and maximum umbilical scarring observed in each clutch. Hatchlings received an individual MonelR identification tag to allow for repeated measures. Hatchlings were kept in the same pans and were again weighed and measured at 10 days post-hatch and the minimum and maximum umbilical scarring were photographed to evaluate the progress of umbilical healing or generation of Table 1 Summary of hatchling weights, umbilical area (mean F S.D.) and decline of umbilical area by clutch and age Clutch ID
Hatch rate (%)
Hatchling weight (g) (day 2)
Hatchling weight (g) (day 10)
Umbilical area (mm2) (day 2)
Umbilical area (mm2) (day 10)
Decline in umbilical area (%)
31 34 35 38 40 301 302 361 362 Total
93 100 100 83 93 90 97 77 70 89
50.68 F 1.47 47.73 F 2.33 54.27 F 2.66 50.04 F 2.82 51.71 F 2.35 47.37 F 3.68 39.59 F 2.16 45.61 F 3.47 55.24 F 3.33 49.02 F 5.26
47.07 F 5.35 49.10 F 2.67 56.23 F 1.81 49.60 F 2.94 53.39 F 2.47 46.81 F 2.95 40.41 F 1.72 50.70 F 3.34 52.10 F 5.31 49.41 F 5.51
59.96 F 23.27 68.50 F 50.06 63.95 F 20.90 109.70 F 32.00 99.09 F 51.03 68.27 F 29.93 69.30 F 23.22 67.92 F 34.48 106.31 F 26.41 78.08 F 38.55
24.59 F 8.37 22.81 F 17.39 18.29 F 4.50 31.44 F 10.81 25.66 F 12.86 21.19 F 7.83 32.78 F 14.14 35.30 F 37.49 49.81 F 16.69 28.24 F 18.23
58.99 66.71 71.40 71.34 74.10 68.96 52.69 48.03 53.15 63.83
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scar tissue. Though not typical of standard farm rearing protocol, animals were not fed at any point during this study. Statistics were generated by two-way repeated measures ANOVA to test for the effects of hatchling age and clutch on umbilical scarring area. The relationship between body weight and umbilical area was tested using regression analysis.
3. Results As there were no significant differences observed in umbilical area and incidence of umbilical scarring between the two incubation sites, data was combined for all subsequent analyses. Results of the two-way repeated measures ANOVA indicated a significant effect of age and clutch on umbilical area ( p < 0.0001, F = 32, R2 = 0.54). Regardless of clutch, there was a significant decline in the umbilical area from days 2 through 10. In fact, the umbilical area decreased from an overall mean of 78 F 39 mm2 at day 2 post-hatch to a mean of 28 F 18 mm2 at 10 days post-hatch represents a decline of almost 64% (Table 1). However, only five of the nine clutches examined expressed a noticeable decline (>50% decrease in umbilical area by day 10, as designated by the authors as an acceptable indices of decline) in the size of this dermal condition (67 – 74%, Table 1). We had hypothesized that bigger hatchlings would have larger umbilical areas and a slower percent decline in this condition during the first few days post-hatch. The differences in umbilical area and percent decline with age across clutches, however, were not associated with differences in hatchling weights. Within clutches and time periods, hatchling weight had no significant effect on the size and/or decline of this condition ( p = 0.5, F = 0.5, R2 = 0.001).
4. Discussion The ability of alligator farmers to limit or eliminate skin imperfections such as umbilical scarring will be crucial in maintaining a sustainable alligator aquaculture program. As demonstrated in this study, the ability to quantify the incidence of umbilical scarring in hatchlings utilizing umbilical area should provide farmers with the capability to evaluate skin quality through quantitative rather than subjective evaluation. This study is the first to examine the incidence of umbilical scarring as it relates to hatchling size and age. Contrary to our hypothesis, the results obtained in this preliminary study suggest that hatchling weight is not a significant driving factor in the incidence/ degree of this dermal condition. The size of the umbilical scarring area, however, decreased significantly during the first 10 days post-hatch. In addition, measurements of the umbilical area at 10 days post-hatch were noticeably less variable across siblings. It remains unknown how long this healing process lasts before no discernable scarring is noticed and future studies should consider a longer monitoring period. It is important to note that hatchlings were not fed during this period and this course of action may have decreased the incidence and degree of scarring. We have noticed that healing occurs at a faster rate when animals are fasted and we recommend not feeding hatchlings specifically: animals with obvious yolk retention
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during the first 2 weeks post-hatch, as this initial fasting allows hatchlings to fully utilize existing yolk reserves. Since no clear relationship was established between the incidence of umbilical scarring as it relates to hatchling weight, we recommend the need for additional trials utilizing larger numbers of clutches to decrease the influence of inter-clutch variability. At this point, the primary cause(s) for this dermal condition remain unknown. However, future studies should consider additional environmental, physiological and management parameters, such as additional incubation temperature trials, examination of fasting versus nonfasting of hatchlings during the first 2 weeks of age, egg and environmental qualities, as well as maternal and genetic influences.
References Deeming, D.C., Ferguson, M.W.J., 1991. Physiological effects of incubation temperature on embryonic development in reptiles and birds. In: Deeming, D.C., Mark, W.J. (Eds.), Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles. Cambridge Univ. Press, Cambridge. Ferguson, M.W.J., 1985. Reproductive biology and embryology of the crocodilians. In: Gans, C., Billet, F. (Eds.), Biology of the Reptilia (Vol. vol. 14 Wiley, New York, NY, pp. 329 – 491. Joanen, T., McNease, L., Ferguson, M.W.J., 1987. The effects of egg incubation temperature on post hatch growth of America alligators. In: Webb, G.J.W., Manolis, S.C., Whitehead, P.J. (Eds.), Wildlife Management: Crocodiles and Alligators. Surrey Beatty Pty, Sydney, pp. 533 – 537. Webb, G.J.W., Manolis, S.C., Otley, B., Heyward, A., 1992. Crocodile management and research in the northern territory: 1990 – 1992. Crocodiles. Proceedings on the 11th Working Meeting of the Crocodile Specialist Group of the Species Survival Commission of the IUCN-The World Conservation Union, Gland, Switzerland, vol. 2, pp. 233 – 275, ISBN 2-8317-0133-3. Wiebe, J.J., Sepu´lveda, M.S., Buckland, J.E., Rauschenberger, H.R., Gross, T.S., unpublished data. American alligator embryonic and hatchling growth and thyroid status in relation to exposure to organochlorine pesticides in central Florida. Submitted to Journal of Environmental Contamination and Toxicology.
Umbilical scarring in hatchling American alligators J.J. Wiebe a,*, M.S. Sepu´lveda b, J.E. Buckland b, S.R. Anderson c, T.S. Gross a,b a
USGS-Florida Integrated Science Center, Center for Aquatic Resource Studies, 7920 N.W. 71st Street, Gainesville, FL 32653, USA b Department of Physiological Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32611, USA c Cypress Creek Farm, Starke, FL 32091, USA Received 23 January 2004; received in revised form 22 March 2004; accepted 24 March 2004 Available online
Abstract Umbilical scarring is the presence of excess scar tissue deposited between abdominal dermal layers at the site of yolk sac absorption in hatchling American alligators (Alligator mississippiensis). The presence of this dermal condition plays a key evaluatory role in the overall quality and subsequent value for various commercial leather products. Despite the prevalent nature of this condition, currently the industry has no standardized protocols for its quantification. The objectives of this study were to examine the relationship between hatchling weight and age and incidence of umbilical scarring and to develop a quantifiable and reproducible technique to measure this dermal condition in hatchling American alligators. Thirty eggs from each of nine clutches were incubated in two separate incubators at different facilities and hatchling umbilical scarring was measured at 2 and 10 days of age using digital calipers. Umbilical area was calculated by multiplying umbilical length times umbilical width. There was a significant effect of both age and clutch on umbilical area (overall decline of 64%) by 10 days post-hatch. However, only five of the nine clutches utilized expressed a noticeable decline in the size of this dermal condition (range 67 – 74%). We had hypothesized that larger hatchlings would have larger umbilical areas and a slower rate of improvement in this condition during the first few days post-hatch. The differences in umbilical area and percent decline with age across clutches, however, were not associated with differences in initial hatchling weights. Within clutches and time periods, hatchling weight had no significant effect on the size and/or rate of decline of this condition. D 2004 Published by Elsevier B.V. Keywords: Umbilical scarring; American alligator hatchlings; Egg quality; Leather goods
* Corresponding author. Tel.: +352-378-8181x400; fax: +352-395-6608. E-mail address: [email protected] (J.J. Wiebe). 0044-8486/$ - see front matter D 2004 Published by Elsevier B.V. doi:10.1016/j.aquaculture.2004.03.027
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1. Introduction In hatchling American alligators (Alligator mississippiensis), umbilical scarring can be defined as the presence of excess scar tissue deposited between abdominal dermal layers at the site of yolk sac absorption. In Florida, licensed alligator farming operations have an estimated 5– 25% incidence of umbilical scarring leading to annual financial losses of approximately US$650,000 (Anderson, unpublished data). Currently, however, there are no standardized protocols available to quantify this dermal condition. Research on alligator production showed eggs at a temperature range of 31.5 –31.7 jC produces hatchlings that grow at an accelerated rate and reduces the incidence of animal hunting (Joanen et al., 1987). At the point of hatching, a hatchling should have absorbed the majority (>95%) of the egg yolk constituents as well as closed the abdominal dermal layer surrounding the yolk sac (Ferguson, 1985). However, accelerated embryonic growth based on incubation temperature may be one of the primary causative agents for the incidence of umbilical scarring and other developmental abnormalities (Deeming and Ferguson, 1991). Differences in alligator embryonic and hatchling growth, however, could also be related to factors other than incubation temperature. Data from our laboratory and others would suggest that, within sites, growth rates can vary significantly across clutches (Webb et al., 1992, Wiebe et al., unpublished data). Among a variety of potential factors, these clutch differences could be the result of genetic influences and/or variations in maternal and subsequent egg nutritional qualities. The objective of the current study was to examine the relationship between hatchling weight and age and incidence of umbilical scarring in the American alligator. We hypothesized that umbilical scarring would be positively related to alligator hatchling weight and that the size of this dermal condition during the first 10 days post-hatch would decrease at a faster rate in leaner animals. An additional objective was to develop a quantifiable and reproducible technique to measure this condition in hatchling American alligators.
2. Materials and methods In order to test the effect of hatchling weight on umbilical scarring, nine clutches collected from a single site in central Florida were utilized due to expected clutch variability on hatchling weight. Thirty eggs from each clutch were divided into equal size (n = 15 eggs/incubation site) and incubated as clutch specific replicates in two different facilities: FISC Florida Integrated Science Center (FISC) and Cypress Creek Farm (CCF) at similar temperature and humidity conditions (31.5 F 1 jC and 95 F 5%, respectively). Eggs were randomized between the two facilities in part to lesson the effect of clutch on future analyses (Fig. 1) (Webb et al., 1992). Eggs were incubated in plastic pans (48 36 16.5 cm) using sphagnum moss as the substrate. Incubation substrate was hydrated at least once a week until hatching. Eggs were left to hatch on their own to limit potential artificial trauma to the umbilical region. Hatch rates were calculated as (number of hatchlings/total number of eggs incubated, Table 1). At 2 days post-hatch, hatchlings
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Fig. 1. Photographic illustration of umbilical scarring at day 2.
were weighed (g), and umbilical scarring was evaluated by measuring umbilical length (distance between the anterior and posterior regions of the umbilical opening) and umbilical width (measured at the median portion of the umbilical region) (Fig. 1). Umbilical area (mm2) was calculated by multiplying umbilical length umbilical width. Umbilical measurements were collected using digital calipers (Mitotoyo, Japan). In addition, a digital photograph was taken of the minimum and maximum umbilical scarring observed in each clutch. Hatchlings received an individual MonelR identification tag to allow for repeated measures. Hatchlings were kept in the same pans and were again weighed and measured at 10 days post-hatch and the minimum and maximum umbilical scarring were photographed to evaluate the progress of umbilical healing or generation of Table 1 Summary of hatchling weights, umbilical area (mean F S.D.) and decline of umbilical area by clutch and age Clutch ID
Hatch rate (%)
Hatchling weight (g) (day 2)
Hatchling weight (g) (day 10)
Umbilical area (mm2) (day 2)
Umbilical area (mm2) (day 10)
Decline in umbilical area (%)
31 34 35 38 40 301 302 361 362 Total
93 100 100 83 93 90 97 77 70 89
50.68 F 1.47 47.73 F 2.33 54.27 F 2.66 50.04 F 2.82 51.71 F 2.35 47.37 F 3.68 39.59 F 2.16 45.61 F 3.47 55.24 F 3.33 49.02 F 5.26
47.07 F 5.35 49.10 F 2.67 56.23 F 1.81 49.60 F 2.94 53.39 F 2.47 46.81 F 2.95 40.41 F 1.72 50.70 F 3.34 52.10 F 5.31 49.41 F 5.51
59.96 F 23.27 68.50 F 50.06 63.95 F 20.90 109.70 F 32.00 99.09 F 51.03 68.27 F 29.93 69.30 F 23.22 67.92 F 34.48 106.31 F 26.41 78.08 F 38.55
24.59 F 8.37 22.81 F 17.39 18.29 F 4.50 31.44 F 10.81 25.66 F 12.86 21.19 F 7.83 32.78 F 14.14 35.30 F 37.49 49.81 F 16.69 28.24 F 18.23
58.99 66.71 71.40 71.34 74.10 68.96 52.69 48.03 53.15 63.83
158
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scar tissue. Though not typical of standard farm rearing protocol, animals were not fed at any point during this study. Statistics were generated by two-way repeated measures ANOVA to test for the effects of hatchling age and clutch on umbilical scarring area. The relationship between body weight and umbilical area was tested using regression analysis.
3. Results As there were no significant differences observed in umbilical area and incidence of umbilical scarring between the two incubation sites, data was combined for all subsequent analyses. Results of the two-way repeated measures ANOVA indicated a significant effect of age and clutch on umbilical area ( p < 0.0001, F = 32, R2 = 0.54). Regardless of clutch, there was a significant decline in the umbilical area from days 2 through 10. In fact, the umbilical area decreased from an overall mean of 78 F 39 mm2 at day 2 post-hatch to a mean of 28 F 18 mm2 at 10 days post-hatch represents a decline of almost 64% (Table 1). However, only five of the nine clutches examined expressed a noticeable decline (>50% decrease in umbilical area by day 10, as designated by the authors as an acceptable indices of decline) in the size of this dermal condition (67 – 74%, Table 1). We had hypothesized that bigger hatchlings would have larger umbilical areas and a slower percent decline in this condition during the first few days post-hatch. The differences in umbilical area and percent decline with age across clutches, however, were not associated with differences in hatchling weights. Within clutches and time periods, hatchling weight had no significant effect on the size and/or decline of this condition ( p = 0.5, F = 0.5, R2 = 0.001).
4. Discussion The ability of alligator farmers to limit or eliminate skin imperfections such as umbilical scarring will be crucial in maintaining a sustainable alligator aquaculture program. As demonstrated in this study, the ability to quantify the incidence of umbilical scarring in hatchlings utilizing umbilical area should provide farmers with the capability to evaluate skin quality through quantitative rather than subjective evaluation. This study is the first to examine the incidence of umbilical scarring as it relates to hatchling size and age. Contrary to our hypothesis, the results obtained in this preliminary study suggest that hatchling weight is not a significant driving factor in the incidence/ degree of this dermal condition. The size of the umbilical scarring area, however, decreased significantly during the first 10 days post-hatch. In addition, measurements of the umbilical area at 10 days post-hatch were noticeably less variable across siblings. It remains unknown how long this healing process lasts before no discernable scarring is noticed and future studies should consider a longer monitoring period. It is important to note that hatchlings were not fed during this period and this course of action may have decreased the incidence and degree of scarring. We have noticed that healing occurs at a faster rate when animals are fasted and we recommend not feeding hatchlings specifically: animals with obvious yolk retention
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during the first 2 weeks post-hatch, as this initial fasting allows hatchlings to fully utilize existing yolk reserves. Since no clear relationship was established between the incidence of umbilical scarring as it relates to hatchling weight, we recommend the need for additional trials utilizing larger numbers of clutches to decrease the influence of inter-clutch variability. At this point, the primary cause(s) for this dermal condition remain unknown. However, future studies should consider additional environmental, physiological and management parameters, such as additional incubation temperature trials, examination of fasting versus nonfasting of hatchlings during the first 2 weeks of age, egg and environmental qualities, as well as maternal and genetic influences.
References Deeming, D.C., Ferguson, M.W.J., 1991. Physiological effects of incubation temperature on embryonic development in reptiles and birds. In: Deeming, D.C., Mark, W.J. (Eds.), Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles. Cambridge Univ. Press, Cambridge. Ferguson, M.W.J., 1985. Reproductive biology and embryology of the crocodilians. In: Gans, C., Billet, F. (Eds.), Biology of the Reptilia (Vol. vol. 14 Wiley, New York, NY, pp. 329 – 491. Joanen, T., McNease, L., Ferguson, M.W.J., 1987. The effects of egg incubation temperature on post hatch growth of America alligators. In: Webb, G.J.W., Manolis, S.C., Whitehead, P.J. (Eds.), Wildlife Management: Crocodiles and Alligators. Surrey Beatty Pty, Sydney, pp. 533 – 537. Webb, G.J.W., Manolis, S.C., Otley, B., Heyward, A., 1992. Crocodile management and research in the northern territory: 1990 – 1992. Crocodiles. Proceedings on the 11th Working Meeting of the Crocodile Specialist Group of the Species Survival Commission of the IUCN-The World Conservation Union, Gland, Switzerland, vol. 2, pp. 233 – 275, ISBN 2-8317-0133-3. Wiebe, J.J., Sepu´lveda, M.S., Buckland, J.E., Rauschenberger, H.R., Gross, T.S., unpublished data. American alligator embryonic and hatchling growth and thyroid status in relation to exposure to organochlorine pesticides in central Florida. Submitted to Journal of Environmental Contamination and Toxicology.