King Penguins in Zoos: Relating Breeding Success to Husbandry Practices



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SUPPLEMENTARY INFORMATION King Penguins in Zoos: Relating Breeding Success to Husbandry Practices Schweizer S., Stoll P., von Houwald F., and Baur B. Supplementary Table S1. Questionnaire Supplementary Table S2. Data of the 39 transition matrices from the Basel Zoo colony. Supplementary Table S3. Results of statistical tests analysing husbandry measures in 12 zoos. Supplementary Table S4. Growth rates of the colony at Basel Zoo without initial years (1980 2011). Supplementary Figure S1. Colony size development at Basel Zoo (1972 2011). Supplementary Figure S2. Annual growth rates at Basel Zoo (1972 2011). Supplementary Figure S3. Detailed relationship between king penguin density and egg productivity for the 11 zoos considered. Supplementary Figure S4. Relation between the deviation from an even sex ratio and mean population size over five years in king penguins at 10 zoos. Supplementary Figure S5. Risk of decline for populations simulated over 25 years with demographic and environmental stochasticity, based on populations with equal, male-biased, and female-biased sex ratios.

Supplementary Table S1. Questionnaire used to gather information of participating zoos. Questionnaire: King Penguin (Aptenodytes patagonicus) Please fill out and return this questionnaire. Name of institution: General 1.) Please attach the ARKS/ZIMS report for your king penguins for the years 2007-2012. 2.) Age of population (years since establishment of a king penguin population): 3.) Please provide the total number of eggs laid by your king penguin population during each year. 2011: 2010: 2009: 2008: 2007: Enclosure 4.) Year king penguins moved into current enclosure: 5.) Please fill out the following table about the king penguin enclosure(s) and indicate m, ft, C, F. Number of pools: Land area (m 2, sq ft): Substrate type (e.g. concrete, sand): Water/pool area (m 2, sq ft): Pool depth (m, ft): Water type/treatment (e.g. salt, chlorine): Water temperature ( C, F ): Air temperature ( C, F): Inside Outside 6.) Other species held in the same enclosure (please include number of individuals of each):

Other 7.) Please describe any show for zoo visitors the king penguins are involved in (e.g. walks) and specify how often this takes place: 8.) Number of months spent outside: Number of hours per day spent outside during those months: 9.) How often are the following used in the enclosure? Disinfectant: Fungicide: 10.) Do all of your king penguins swim regularly? yes no 11.) Do you provide snow or ice in your exhibit? yes no 12.) Does the enclosure have any incoming natural light? yes no 13.) Is the lighting varied between winter and summer? yes no 14.) Are incubating king penguins fed by keepers? yes no 15.) Who incubates the egg? parent incubator 16.) How are chicks reared? parent hand

Supplementary Table S2. Data of the 39 transition matrices from the Basel Zoo colony. Year Total Ratio m f s c f t+1 s t+1 c t+1 c -> s s -> f P 13 P 21 P 22 P 32 P 33 1972 4 0.75 3 1 0 0 1 0 0 0 0 0 0 0 0 1 1973 4 0.75 3 1 0 0 1 0 0 0 0 0 0 0 0 1 1974 4 0.75 3 1 0 0 2 0 0 0 0 0 0 0 0 1 1975 7 0.71 5 2 0 0 3 0 0 0 0 0 0 0 0 1 1976 8 0.62 5 3 0 0 3 0 0 0 0 0 0 0 0 1 1977 8 0.62 5 3 0 0 3 0 0 0 0 0 0 0 0 1 1978 8 0.62 5 3 0 0 3 0 0 0 0 0 0 0 0 1 1979 8 0.62 5 3 0 0 3 0 0 0 0 0 0 0 0 1 1980 8 0.62 5 3 0 0 3 0 1 0 0 0.33 0 0 0 1 1981 9 0.62 5 3 0 1 1 1 2 1 0 0.67 1 0 0 0.33 1982 9 0.83 5 1 1 2 1 2 1 2 0 1 1 0 0 1 1983 8 0.80 4 1 2 1 1 3 1 1 0 1 1 1 0 1 1984 9 0.80 4 1 3 1 2 2 1 1 1 1 1 0.50 0.50 1 1985 10 0.71 5 2 2 1 3 2 1 1 1 0.50 1 0.50 0.50 1 1986 11 0.62 5 3 2 1 3 2 0 1 0 0 1 1 0 1 1987 11 0.67 6 3 2 0 4 1 3 0 1 1 0 0.50 0.50 1 1988 13 0.56 5 4 1 3 5 0 1 0 1 0.25 0 0 1 1 1989 10 0.44 4 5 0 1 5 1 1 1 0 0.20 1 0 0 1 1990 11 0.44 4 5 1 1 5 2 0 1 0 0 1 1 0 1 1991 11 0.44 4 5 2 0 6 1 0 0 1 0 0 0.50 0.50 1 1992 11 0.40 4 6 1 0 6 0 2 0 0 0.33 0 0 0 1 1993 13 0.46 5 6 0 2 6 1 2 1 0 0.33 0.50 0 0 1 1994 14 0.46 5 6 1 2 6 3 4 2 0 0.67 1 1 0 1 1995 17 0.40 4 6 3 4 6 5 3 4 0 0.50 1 0.50 0 1 1996 19 0.46 5 6 5 3 5 6 0 3 0 0 1 0.75 0 0.83 1997 17 0.55 6 5 6 0 5 0 3 0 0 0.60 0 0.00 0 1 1998 15 0.58 7 5 0 3 4 3 2 3 0 0.40 1 0 0 0.80 1999 16 0.64 7 4 3 2 3 5 2 2 0 0.50 1 1 0 0.75 2000 17 0.70 7 3 5 2 3 2 0 1 1 0 0.50 0.50 0.50 0.67 2001 9 0.57 4 3 2 0 4 1 0 0 1 0 0 0.50 0.50 1 2002 9 0.50 4 4 1 0 5 0 2 0 1 0.50 0 0 1 1 2003 11 0.44 4 5 0 2 5 2 1 2 0 0.20 1 0 0 1 2004 12 0.44 4 5 2 1 4 3 0 1 0 0 1 1 0 0.80 2005 11 0.50 4 4 3 0 5 1 0 0 1 0 0 0.50 0.50 1 2006 11 0.50 5 5 1 0 5 0 2 0 0 0.40 0 0 0 1 2007 13 0.55 6 5 0 2 5 0 2 0 0 0.40 0 0 0 1 2008 13 0.55 6 5 0 2 6 2 3 2 0 0.60 1 0 0 1 2009 17 0.50 6 6 2 3 6 0 2 0 0 0.33 0 0 0 1 2010 15 0.54 7 6 0 2 6 0 1 0 0 0.17 0 0 0 1 Transition matrix Mean matrix c s f P 13 P 21 P 22 P 32 P 33 0 0 P 13 c 0 0 0.30 mean 0.30 0.44 0.28 0.14 0.95 P 21 P 22 0 s 0.44 0.28 0 SD 0.33 0.49 0.38 0.28 0.13 0 P 32 P 33 f 0 0.14 0.95 Lambda = 0.981 The term Total refers to the total colony size including males (m), females (f), subadults (s), and chicks (c). Ratio is the adult sex ratio (m/(m+f) ). c -> s refers to the number of chicks becoming subadults and s -> f is the number of subadults becoming females that year. P 13 is the rate at which a female will produce a chick, P 21 the probability at which a chick becomes a subadult, and so on.

Supplementary Table S3. Results of statistical tests analysing husbandry measures in 12 zoos. Linear regressions Dependent variable Independent variable r 2 Statistic P Egg productivity King penguin density 1 0.40 F 1,9 = 6.0 0.037 Hatching success King penguin density 1 0.011 F 1,9 = 0.10 0.76 Chick survival King penguin density 1 0.17 F 1,9 = 1.8 0.21 Chick productivity King penguin density 1 0.27 F 1,9 = 3.3 0.10 Egg productivity Total density 1 0.34 F 1,9 = 4.7 0.058 Hatching success Total density 1 0.0016 F 1,9 = 0.014 0.91 Chick survival Total density 1 0.25 F 1,9 = 3.0 0.12 Chick productivity Total density 1 0.14 F 1,9 = 1.4 0.26 Egg productivity Dev. from even sex ratio 2 0.59 F 1,8 = 11 0.0096 Hatching success Dev. from even sex ratio 2 0.021 F 1,8 = 0.17 0.69 Chick survival Dev. from even sex ratio 2 0.23 F 1,8 = 2.5 0.16 Chick productivity Dev. from even sex ratio 2 0.18 F 1,8 = 1.8 0.22 1 In density analyses, Wuppertal was excluded as its population switched enclosures in the midst of the study. 2 Vienna and Wuppertal were excluded from sex ratio analyses, as they did not have all of the penguins sexed. Wilcoxon rank sum tests Dependent variable Comparison Statistic P Hatching success Incubated by parent (n = 9) / incubated artificially (n = 3) W = 14 1 Chick survival Raised by parent(s) (n = 10) / raised by hand (n = 2) W = 14 0.45 Egg productivity Interactive show (n = 5) / no interactive show (n = 7) W = 24 0.34 Hatching success Interactive show (n = 5) / no interactive show (n = 7) W = 26 0.19 Chick survival Interactive show (n = 5) / no interactive show (n = 7) W = 25.5 0.22 Chick productivity Interactive show (n = 5) / no interactive show (n = 7) W = 30 0.051 Egg productivity Outside walk (n = 4) / no outside walk (n = 8) W = 18 0.81 Hatching success Outside walk (n = 4) / no outside walk (n = 8) W = 29 0.028 Chick survival Outside walk (n = 4) / no outside walk (n = 8) W = 19 0.67 Chick productivity Outside walk (n = 4) / no outside walk (n = 8) W = 25 0.15 Egg productivity Swim regularly (n = 8) / some or all never swim (n = 4) W = 14 0.81 Hatching success Swim regularly (n = 8) / some or all never swim (n = 4) W = 25 0.15 Chick survival Swim regularly (n = 8) / some or all never swim (n = 4) W = 21 0.44 Chick productivity Swim regularly (n = 8) / some or all never swim (n = 4) W = 19.5 0.61 Egg productivity Fungicide use (n = 3) / no fungicide used (n = 9) W = 23 0.1 Hatching success Fungicide use (n = 3) / no fungicide used (n = 9) W = 15 0.86 Chick survival Fungicide use (n = 3) / no fungicide used (n = 9) W = 14 1 Chick productivity Fungicide use (n = 3) / no fungicide used (n = 9) W = 21 0.19 Egg productivity Disinfectant use (n = 6) / no disinfectant used (n = 6) W = 22 0.59 Hatching success Disinfectant use (n = 6) / no disinfectant used (n = 6) W = 16 0.82 Chick survival Disinfectant use (n = 6) / no disinfectant used (n = 6) W = 16.5 0.87 Chick productivity Disinfectant use (n = 6) / no disinfectant used (n = 6) W = 20 0.81 Egg productivity Natural light (n = 7) / no natural light (n = 5) W = 10 0.27 Hatching success Natural light (n = 7) / no natural light (n = 5) W = 21 0.64 Chick survival Natural light (n = 7) / no natural light (n = 5) W = 14 0.62 Chick productivity Natural light (n = 7) / no natural light (n = 5) W = 10.5 0.29 Egg productivity Salt water (n = 7) / only freshwater (n = 5) W = 13 0.53 Hatching success Salt water (n = 7) / only freshwater (n = 5) W = 9 0.20 Chick survival Salt water (n = 7) / only freshwater (n = 5) W = 21.5 0.57 Chick productivity Salt water (n = 7) / only freshwater (n = 5) W = 14.5 0.68

Supplementary Table S4. Growth rates of the king penguin colony at Basel Zoo for average matrix over 31 annual transitions and average matrices of years with different colony sizes and adult sex ratios (excluding first eight years with no reproduction) n Deterministic λ Stochastic approximate λ Stochastic simulated λ 95% confidence interval Mean matrix 31 0.999 0.986 0.977 0.970 0.983 Colony size > 15 6 0.913 0.910 0.905 0.900 0.910 Colony size 10 to 15 18 1.016 1.012 1.008 1.003 1.013 Colony size < 10 7 1.039 1.002 0.981 0.972 0.990 Equal sex ratios 4 1.000 1.000 1.000 0.996 1.004 Male biased 17 0.999 0.979 0.963 0.955 0.970 Female biased 10 0.980 0.976 0.975 0.970 0.979 n = number of matrices, λ = growth rate, 95% confidence interval based on 10,000 simulations

Supplementary Figure S1. Colony size development at Basel Zoo (1972 2011). The decrease in number of individuals in the year 2001 is due to an outbreak of Aspergillosis.

Supplementary Figure S2. Annual growth rates at Basel Zoo (1972 2011). Lambda (λ) is the growth rate at stable stage distribution while N t / N t-1 is the currently observed rate of growth. The relatively large deviations in 1974 and 1984, along with most smaller ones, are due to incoming females and subadults maturing to females.

Supplementary Figure S3. Detailed relationship between mean egg productivity and king penguin density for the 11 zoos considered. The crosses show 95% confidence intervals.

Edinburgh 0.3 Deviation from even sex ratio 0.2 0.1 Munich Cincinnati Antwerp r² = 0.37, n = 10, P = 0.065 Zurich Rotterdam Omaha Basel 0 Odense Moody 0 10 20 30 Mean population size Supplementary Figure S4. Relation between the deviation from an even sex ratio and mean population size over five years in king penguins at 10 zoos. The line shows a marginally significant exponential (y = 0.358e -0.117 x ) fit.

Supplementary Figure S5. Risk of decline for populations simulated over 25 years with demographic and environmental stochasticity, based on populations with equal (black line), male-biased (red line), and female-biased (green) sex ratios. The y-axis gives the probability that the population size will fall below a certain threshold on the x-axis. Dotted lines give approximate 95% confidence intervals constructed by replicating sets of 100 stochastic simulations 100 times.