SUPPLEMENTARY MATERIAL
The impact of ovulation mode on sperm quantity and quality in mammals
Carl D. Soulsbury and Graziella Iossa
Appendix A
Data used for PGLM analysis including sperm concentration (106 ml-1), ejaculate
volume (ml), total motile sperm (106) per ejaculate, % sperm motility, % normal sperm
morphology and ovulation mode (SPO: spontaneous; IND: induced). ND = no data.
Appendix B
Results of phylogenetically corrected general linear models comparing (i) sperm
concentration (ii) ejaculate volume, (iii) % sperm motility and (iv) % normal sperm
with source of sample (captive, captive-born, mixture of captive and wild, wild, wildborn).
Appendix C
Alternative models that are stongly supported ΔAICc<2 showing (i) sperm
concentration (ii) ejaculate volume, (iii) % sperm motility and (iv) % normal sperm and
associated significant variables.
APPENDIX A
Species
Acinonyx jubatus
Ailuropoda melanoleuca
Alcelaphus buselaphus
Alopex lagopus
Alouatta caraya
Ammotragus lervia
Ateles fusciceps
Ateles geoffroyi
Axis axis
Bison bison
Bison bonasus
Bos grunniens
Bradypus tridactylus
Callithrix_jacchus
Camelus bactrianus
Camelus dromedarius
Canis familiaris
Canis latrans
Canis lupus
Canis rufus
Capreolus capreolus
Capricornis sumatensis
Cebus apella
Ceratotherium simum
Cercocebus galeritus
Cercopithecus aethiops
Sperm
concentration
(106 ml-1)
Ejaculate
volume
(ml)
Total motile
sperm (106)
per ejaculate
%
sperm
motility
%
normal
sperm
Ovulation
modea
21.9
5420.0
1373.0
317.0
649.5
4012.0
274.2
ND
338.0
711.3
5030.0
1552.0
91.9
ND
414.0
556.0
293.3
193.0
271.1
146.5
485.7
515.8
92.9
164.5
575.5
117.0
2.10
5.02
4.50
0.98
0.09
2.00
1.25
ND
4.10
3.00
9.50
3.58
0.05
0.03
8.20
6.70
2.20
1.00
7.00
4.70
1.05
2.3
0.65
29.86
1.30
0.86
46.0
27208.4
2471.4
310.7
44.3
7221.6
ND
ND
921.6
1468.1
NA
ND
NA
ND
2118.4
ND
645.3
193.0
1897.7
688.6
397.8
715.4
14.5
4057.0
448.9
55.3
0.69
0.80
0.4
0.73
0.757
0.9
ND
0.9
0.665
0.688
ND
ND
ND
0.48
0.624
ND
0.84
0.75
0.89
0.71
0.78
0.60
0.24
0.826
0.6
0.55
0.18
0.73
0.42
0.81
0.787
0.96
ND
ND
0.791
0.738
ND
ND
ND
0.49
ND
ND
0.76
0.79
0.78
0.74
0.7
0.71
ND
ND
ND
0.94
INDb
SPOb
SPO
SPOb
SPO
ND
SPO
SPO
SPO
SPO
SPO
SPO
SPO
SPO
IND
IND
SPOb
SPOb
SPOb
SPOb
SPOb
ND
SPO
SPO
SPO
SPO
References
Crosier et al. (2007)
Olson et al. (2003)
Metrione et al. (2008b)
Barta (1999)
Valle et al. (2004)
Meija et al. (2009)
Møller (1989)
Kraemer and Kuehl (1980); Møller (1989)
Mylrea et al. (1999): Umapathy et al. (2001)
Matsuda et al. (1996); Helbig et al. (2007)
Pérez-Garnelo et al. (2001)
Sarkar and Prakash (2005); Sarkar et al. (2009)
Mühlbauer et al. (2006); Peres et al. (2008)
Cui et al. (1991)
Chen et al. (2005); Mosaferi et al. (2005)
Hombach-Klonisch et al. (2000): Agarwal et al. (2004)
Ortega-Pacheco et al. (2006)
Green et al. (1984); Minter and DeLiberto (2008)
Zindl (2006)
Goodrowe et al. (1998)
Goeritz et al. (2003); Santiago-Moreno et al. (2006)
Suwanpugdee et al. (2009)
Møller (1989)
Radcliffe et al. (1997); Reid et al. (2009)
Møller (1989)
Seier et al. (1989)
Cervus elaphus
Cervus eldii
Chinchilla lanigera
Chrysocyon brachyurus
Connochaetes taurinus
Dama dama
Dasyprocta leporina
Dicerorhinus sumatrensis
Diceros bicornis
Elephas maximus
Equus asinis
Equus burchelli
Equus ferus
Erythrocebus pathas
Euphractus sexcinctus
Felis catus
Felis concolor
Felis manul
Felis margarita
Gazella cuvieri
Gazella dama
Gazella dorcas
Gorilla gorilla
Herpailurus yaguarondi
Homo sapiens
Hylobates lar
Hylobates moloch
Lagenorhynchus obliquidens
Lama guanaco
Lama paco
Leopardus pardalis
440.0
ND
483.0
29.5
352.0
3009.0
106.7
24.6
23.7
1295.0
294.0
74.8
100.5
1153.4
45.0
167.6
15.6
123.0
209.8
167.6
402.6
1068.8
381.4
142.7
7.2
63.5
152.4
ND
625.0
5.5
72.4
53.8
ND
1.80
0.09
2.00
11.25
3.00
0.70
104.00
59.00
30.00
67.60
34.10
19.90
0.60
0.35
0.12
2.05
0.21
0.20
0.12
2.86
1.35
1.80
0.52
0.08
4.30
1.30
ND
7.7
2.41
1.60
0.62
NA
NA
44.7
59.0
2376.0
7673.0
ND
1535.0
560.0
10501.2
14309.6
765.2
1054.0
311.4
9.69
20.8
32.0
25.8
17.0
26.5
843.7
1155.2
588.3
37.0
0.6
163.8
17.8
NA
4382.0
3.1
91.3
33.4
0.8
0.8
0.98
0.65
0.6
0.85
ND
0.6
0.4
0.270
0.72
0.3
0.527
0.45
0.61
0.84
0.61
0.79
0.404
0.844
0.732
0.8
0.857
0.497
0.58
0.6
0.09
0.05
0.92
0.24
0.79
0.71
0.812
0.967
ND
0.50
ND
ND
ND
0.40
0.29
0.788
0.88
ND
0.234
ND
0.86
0.72
0.34
0.63
0.596
0.716
0.866
ND
0.89
ND
0.26
ND
ND
ND
ND
0.61
NA
0.58
SPO
SPO
SPO
INDb
ND
SPO
SPO
IND
SPO
SPO
SPO
SPO
SPO
SPO
ND
INDb
INDb
INDb
IND
IND
ND
ND
ND
SPO
INDb
SPO
SPO
SPO
ND
IND
IND
INDb
Martínez et al. (2008)
Hosack et al. (1999); Harnal et al. (2001)
Spotorno et al. (2004); Busso et al. (2005)
Baker et al. (2007)
Watson (1976)
Asher and Smith (1987); Meija et al. (2009)
Weir (1974); Mollineau et al. (2008)
O’Brien and Roth (2000); Roth et al. (2001)
Radliffe et al. (2001); Roth (2006)
Czekala et al. (2003); Thongtip et al. (2008)
Asa (2002); Cortés-Gutiérrez et al. (2008)
Crump and Crump (1994); Asa (2002)
Asa (2002); Collins et al. (2006)
Møller (1989)
Serafim et al. (In press)
Howard et al. (1990)
Swanson et al. (2003)
Swanson et al. (1996)
Herrick et al. (In press)
Herrick et al. (In press)
Garde et al. (2008)
Abaigar et al. (2001)
Howard et al. (1983)
Kraemer and Kuehl (1980); Møller (1989)
Swanson et al. (2003)
Møller (1989)
Møller (1989)
Kraemer and Kuehl (1980); Møller (1989)
Robeck et al. (In press)
Tibary and Vaughan (2006): Giuliano et al. (2008)
Bravo et al. (1997); Tibary and Vaughan (2006)
Swanson et al. (2003)
Leopardus tigrinus
Leopardus wiedii
Lepus europaeus
Litocranius walleri
Lontra canadensis
Loxodonta africana
Lycaon pictus
Lynx lynx
Lynx rufus
Macaca arctoides
Macaca assamensis
Macaca cyclopsis
Macaca fascicularis
Macaca fuscata
Macaca mulatta
Macaca nemestrina
Macaca radiata
Macaca thibetana
Marmota monax
Martes pennanti
Microcebus murinus
Mus musculus
Mustela furo
Mustela nigripes
Mustela vison
Myocastor coypu
Nasua nasua
Neofelis nebulosa
Oncifelis colocolo
Oncifelis geoffroyi
Orcinus orca
Oryctolagus cuniculus
83.0
14.2
248.0
1146.8
348.8
2408.6
212.3
8.0
24.4
468.0
1150.0
366.0
402.8
348.5
613.9
276.9
434.0
4560.0
2.8
2073.0
NA
160.3
706.1
1030.9
178.6
730.0
60.0
27.5
364.0
66.5
98.8
238.9
0.11
0.31
0.59
0.90
0.53
93.30
0.60
0.28
0.36
1.60
3.20
ND
1.02
2.36
1.43
1.27
1.80
6.30
0.15
0.03
NA
0.004
0.05
0.01
0.02
0.91
0.06
0.64
0.08
0.21
13.90
0.50
9.1
4.4
109.7
619.3
186.3
157305.7
127.4
2.2
4.9
366.9
NA
NA
267.8
666.2
635.6
316.5
468.7
NA
0.3
68.4
NA
NA
35.3
13.3
3.8
434.5
2.6
17.6
29.1
14.0
12428.5
87.0
0.32
0.63
0.75
0.6
0.88
0.7
0.70
0.77
0.56
0.49
ND
ND
0.655
0.81
0.726
0.9
0.6
ND
0.61
0.78
0.484
ND
0.81
0.59
0.60
0.654
0.68
0.71
0.81
0.64
0.905
0.728
0.36
0.40
ND
0.4
0.86
0.775
0.76
0.26
0.15
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
0.67
0.53
ND
0.919
0.85
0.61
0.57
0.17
0.884
0.83
INDb
SPOb
IND
SPO
INDb
SPO
SPOb
INDb
INDb
SPO
SPO
SPO
SPO
SPO
SPO
SPO
SPO
SPO
IND
INDb
SPO
SPO
INDb
INDb
INDb
IND
ND
IND
INDb
INDb
SPO
IND
Swanson et al. (2003)
Swanson et al. (2003)
Kozdrowski and Dubiel (2005); Kozdrowski and Siemieniuch (2009)
Penfold et al. (2005)
Bateman et al. (2005)
Howard et al. (1984); Hermes et al. (2000)
Johnston et al. (2007)
Jewgenow et al. (2006)
Gañán et al. (2009)
Møller (1989)
Yang et al. (1994)
Møller (1989)
Kraemer and Kuehl (1980); Møller (1989)
Møller 1989)
Kraemer and Kuehl (1980); Møller (1989)
Kraemer and Kuehl (1980); Møller (1989)
Kraemer and Kuehl (1980); Møller (1989)
Yang et al. (1994)
Concannon et al. (1996); Sinha Hikim et al. (1992)
Frost et al. (1997)
Aslam et al. (2002)
Allen (1922); Snyder (1966)
Howard et al. (1991)
Wolf et al. (2000)
Aulerich et al. (1972)
Brown (1975); Qingjie et al. (1997)
Lima et al. (2009)
Wildt et al. (1986); Brown et al. (1995)
Swanson et al. (2003)
Swanson et al. (2003)
Robeck et al. (2004); Katsumata et al. (2006)
Staples (1967); Taha et al. (2006)
Oryx dammah
Ovis canadensis
Ovis musimon
Pan paniscus
Pan troglodytes
Panthera leo
Panthera onca
Panthera pardus
Panthera tigris
Panthera uncia
Papio anubis
Papio cynocephalus
Parahyena brunnea
Pongo pygmaeus
Presbytis entellus
Prionailurus bengalensis
Prionailurus viverrinus
Pteropus alecto
Pteropus poliocephalus
Pteropus scapulatus
Rhinoceros unicornis
Rupicapra pyrenaica
Saguinus mystax
Saguinus nigricollis
Spilogale gracilis
Spilogale putorius
Sus scrofa
Syncerus caffer
Tayassu tajacu
Theropithecus gelada
Thryonomys swinderianus
Tolypeutes matacus
780.0
3031.0
3009.0
821.0
370.6
12.3
4.3
55.8
38.1
38.7
76.7
143.5
270.0
67.1
170.4
37.0
108.0
397.0
477.0
291.0
27.2
1.6
195.5
833.3
63.0
112.7
300.0
461.5
371.0
502.9
0.9
23.0
7.70
1.40
1.20
1.80
2.02
6.00
6.29
1.57
5.70
2.00
ND
3.60
2.00
1.10
2.70
0.15
0.50
0.09
0.04
0.03
81.00
0.60
ND
0.03
0.13
0.02
180.00
22.20
1.10
1.00
95.0
0.14
4654.7
3479.6
3069.2
1108.4
311.4
73.8
27.1
87.6
217.2
77.4
ND
232.5
540.0
34.7
358.4
5.5
54.0
28.0
12.3
4.2
1144.0
0.7
ND
ND
8.1
2.2
43200.0
8370.0
ND
105.6
53.9
0.8
0.775
0.82
0.85
0.75
0.417
0.89
0.66
0.57
0.77
0.57
0.563
0.45
0.80
0.47
0.779
0.74
0.73
0.75
0.594
0.556
0.52
0.696
0.42
ND
0.56
0.71
0.8
0.817
ND
0.21
0.63
0.245
0.76
0.89
0.95
ND
ND
0.72
0.57
0.72
0.60
0.41
ND
ND
ND
ND
0.727
0.65
0.34
ND
0.59
0.555
0.34
0.968
ND
ND
0.70
0.35
ND
0.913
0.553
ND
ND
0.869
SPO
ND
SPO
SPO
SPO
INDb
INDb
IND
IND
INDb
SPO
SPO
SPO
SPO
SPO
IND
INDb
SPO
SPO
SPO
SPO
ND
SPO
SPO
SPOb
SPOb
SPO
SPO
SPO
SPO
IND
ND
Roth et al. (1998); Morrow et al. (1999)
Meija et al. (2009)
Gómez-Brunet et al. (2008); Meija et al. (2009)
Kraemer and Kuehl (1980); Møller (1989)
Kraemer and Kuehl (1980); Møller (1989)
Brown et al. (1991a)
Swanson et al. (2003)
Schmidt et al. (1988); Jayaprakash et al. (2001)
Seal et al. (1985); Byers et al. (1990)
Johnston et al. (1994)
Kraemer and Kuehl (1980); Amboka and Mwethera (2003)
Møller (1989)
Ensley et al. (1982)
Kraemer and Kuehl (1980); Møller (1989)
Lohiya et al. (1998)
Howard and Wildt (1990)
Thiangtum et al. (2006)
Martin and Bernard (2000); Melville et al. (2008)
Martin and Bernard (2000); de Jong et al. (2005)
Martin and Bernard (2000); de Jong et al. (2005)
Stoops et al. (2004); Roth (2006)
Carluccio et al. (2007)
Møller (1989)
Møller (1989)
Kaplan and Mead (1993)
Kaplan and Mead (1994)
Kozdrowski and Andrzej Dubiel (2004)
Brown et al. (1991b)
Hellgren et al. (1989); Santos et al. (2006)
Møller 1989; Kraemer and Kuehl 1980
Addo et al. (2002); Soro et al. (2009)
Herrick et al. (2002)
Tragelaphus strepsiceros
Tragulus javanicus
Tupaia glis
Tursiop aduncus
Tursiops truncatus
Ursus arctos
Ursus thibetanus
Vulpes vulpes
a
375.2
366.9
103.2
506.0
964.0
471.6
1049.0
63.6
4.40
0.02
0.10
31.2
11.50
2.70
0.61
1.60
ND
3.5
ND
13671.7
9800.0
1273.3
639.9
101.8
0.59
0.4
ND
0.87
0.884
0.80
0.64
0.65
0.57
0.712
ND
ND
0.992
0.78
0.63
0.77
ND
ND
IND
SPO
SPO
INDb
IND
SPOb
Schiewe et al. (1991)
Haron et al. (2000)
Conaway and Sorenson (1966); Kraemer and Kuehl (1980)
Brook (2001); Yuen et al. (In press)
Kirkby and Ridgway (1984); Robeck et al. (2005)
Pérez-Garnelo et al. (2005)
Kojima et al. (2001); Boone et al. (2007)
Brzozowski (1984)
all primates are classified as spontaneous ovulators (Bercovitch & Zeigler 2002), b Iossa et al. (2008)
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APPENDIX B
Model
MLλ
Sperm concentration
0.73a,b Captive
Ejaculate volume
Variable
% sperm with normal morphology
t
P
r
CI
0
Captive-born
0.11
-0.41
0.69
-0.04
-0.21/0.14
Mixture
-0.02
-0.10
0.92
-0.01
-0.18/0.17
Wild
0.05
0.23
0.82
0.02
-0.16/0.20
Wild-caught
0.00
0.03
0.98
0.00
-0.17/0.18
0.74
13.14
<0.01
0.77
0.69/0.82
0.75a,b Body mass
Captive
% sperm motility
Slope
0
Captive-born
-0.29
-0.59
0.56
-0.05
-0.22/0.12
Mixture
-0.19
-0.47
0.64
-0.04
-0.22/0.14
Wild
-0.13
-0.37
0.71
-0.03
-0.21/0.14
Wild-caught
0.24
0.75
0.46
0.07
-0.11/0.24
0.58a,b Captive
0
Captive-born
-9.81
-1.34
0.18
-0.13
-0.30/0.06
Mixture
0.11
0.02
0.98
0.00
-0.18/0.18
Wild-caught
6.87
1.64
0.11
0.15
-0.03/0.32
Wild
-2.33
-0.60
0.55
-0.06
-0.23/0.13
0.59a,b Captive
0
Captive-born
12.49
0.82
0.41
0.09
-0.13/0.31
Mixture
-0.66
-0.10
0.92
-0.01
-0.23/0.21
Wild-caught
-3.30
-0.69
0.49
-0.08
-0.29/0.15
Wild
-2.64
0.56
0.58
0.06
-0.16/0.28
APPENDIX C
Model
MLλ
AICc
Variable
Sperm concentration
Ejaculate volume
0.71a,b
314.08 Body mass
0.71
r
CI
12.53
<0.01
0.77
0.69/0.82
0
Mating system: SM
0.65
1.68
0.10
0.16
-0.03/0.33
Mating system: SP
-0.33
-1.52
0.13
-0.14
-0.32/0.04
0.95
0.34
0.09
-0.10/0.27
-0.63
0.53
-0.06
-0.25/0.13
No model strongly supported
0.69a,b
545.38 Ovulation: IND
0.59a,b
808.07 Length of mating season: long
Length of mating season: short
a
P
Mating system: MM
Ovulation: SPO
% normal sperm
t
No model strongly supported
Total motile sperm per ejaculate
% sperm motility
Slope
significantly different from 0, b significantly different from 1
0
3.59
0
1.46