Alces39_89.pdf ALCES VOL. 39, 2003 NYGRÉN – MULTIPLE FECUNDITY IN MOOSE 89 THE POTENTIAL FOR MULTIPLE FECUNDITY OF MOOSE IN FINLAND Tuire Nygrén Finnish Game and Fisheries Research Institute, Ilomantsi Game Research Station, FI-82900 Ilomantsi, Finland ABSTRACT: Multiple fecundity (i.e., >2 fetuses or calves per female) is a rare and poorly known phenomenon in moose (Alces alces). In this paper I: (1) report the frequency of multiple fecundity of moose in Finland; (2) study the frequencies of multiple fecundity in different years and areas; (3) discuss the viability of litters with different numbers of progeny; and (4) discuss the possible fecundity effects of selective harvest and the evolutionary aspects of multiple fecundity. The embryo numbers of harvested cows were counted during 1980-89 (n = 2,347) and the proportion of single, twin, and triplet calves were determined from the 1986-99 moose observation material recorded in the field by hunters during the hunting season (n = 585,149). The material includes 4 sets of quadruplet calves, 1 set of stillborn sextuplets, and a moose female with 5 sets of triplet calves; a total of 30 calves in 15 years. In Finland, 60.38 % of pregnant moose cows had one, 39.37% two, 0.21% three, and 0.04% four embryos. In the observation material, 61.79% of the cows had one calf, 38.18% twin calves, and 0.03% triplet calves. The proportion of multiple cases decreased from south to north. The viability of single and twin calves was found to be very high, but only 15% of the sets of triplet calves seemed to survive up to the first fall. Calf survival rate was clearly higher in 1980-99 than in 1963-66, possibly depending on the different age structures of the female populations. According to the literature, the frequency of multiple fecundity in moose appears to be lower in North American than European moose populations. ALCES VOL. 39: 89-107 (2003) Key words: Alces alces, calf survival, fecundity, moose, multiple fecundity, quadruplet calves, reproduction, sextuplet calves, triplet calves, twinning In favorable conditions, the reproduc- tive potential of a moose (Alces alces) population can be very high (Markgren 1969, Stålfelt 1974, Nygrén 1983, Cederlund and Sand 1991, Danilkin and Ulitin 1998, Schwartz 1998). Most females annually produce either single or twin calves. The non-reproducers are pubescent females (1- 2 years old), very old cows (15-20 years), or females unable to give birth every year while living on the poor forage or harsh conditions of the North (Peek 1962, Blood 1974, Markgren 1974, Albright and Keith 1987). The most productive females can give birth to as many as 3 (Peterson 1955, Heptner et al. 1966, Danilkin 1999) or 4 calves (Skuncke 1949, Knorre 1959, Ling 1974, Martin 1989, Vitakova and Minajev 2000). In different moose populations the pro- portion of singles and twins varies (Markgren 1969, Mech et al. 1987, Boer 1992, Gasaway et al. 1992, Danilkin and Ulitin 1998, Schwartz 1998) but in all moose populations multiple fecundity (i.e., >2 fetuses or calves per single moose female) is a very rare phenomenon (Pimlott 1959, Heptner et al. 1966, Franzmann 1981, Kozlo 1983, Schwartz 1998). In addition, the number of reports of triplet or quadruplet sets is small (Table 1) and analytical papers dealing with the maximal productivity of moose are prac- tically nonexistent. Ling (1974) and Kozlo (1983) might be the only authors who report MULTIPLE FECUNDITY IN MOOSE – NYGRÉN ALCES VOL. 39, 2003 90 T ab le 1 . R ep or ts o f m ul ti pl e fe cu nd it y ca se s in fe m al e m oo se ( A lc es a lc es ). R eg io n1 M et ho d2 Sa m pl e N um be r O f % N um be r O f A ut ho r Si ze 3 T ri pl et s T ri pl et s Q ua dr up le ts N A 1 - + - - Se to n (1 92 7) c it ed b y Pe te rs on (1 95 5) N A , A la sk a 1 - 1 - - H os le y an d G la se r ( 19 52 ) N A , O nt ar io 1 - 3 - - Pe te rs on (1 95 5) N A , N ew fo un dl an d 3 1, 57 9 2 0. 13 - Pi m lo tt (1 95 9) N A , I sl e R oy al e 1 - 1 - - M ol l a nd M ol l ( 19 76 ) c it ed b y M ar ti n (1 98 9) N A , A la sk a 3 3, 31 4 2 0. 06 - B ai le y an d B an gs (1 98 0) N A , A la sk a 1 - 1 - - Fr an zm an n (1 98 1) N A , A la sk a 3 - 1 - - Fr an zm an n an d Sc hw ar tz (1 98 5) N A , I sl e R oy al e 1 - 1 - 1 M ar tin (1 98 9) RU 1 - 1 - - B ut ur li n (1 89 0) c it ed b y T im of ej ev a (1 97 4) R U , K om i 2 - >2 - 1 K no rr e ( 19 59 ) R U , T at ar sk ij 2 - 3 - - Z ar ip ov a nd Z na m en sk ij i ( 19 64 ) c it ed b y H er uv im ov (1 96 9) R U , L en in gr ad 2 2, 13 9 4 0. 19 - D em en te v (1 96 7) c it ed b y L in g (1 97 4) R U , K ir ov 2 - 1 - - Pa vl ov a nd Ja za n (1 96 7) c it ed b y T im of ej ev a (1 97 4) R U , V la di m ir 2 58 1 1. 72 - Sy so je v (1 96 7) c it ed b y L in g (1 97 4) R U M os co w 3 24 8 1 0. 40 - M ak ar ov a (1 96 9) c it ed b y L in g (1 97 4) R U T am bo v 2a 14 1 2 1. 42 - H er uv im ov (1 96 9) R U , L en in gr ad 2 1, 85 0 4 0. 22 - N ov ik ov (1 97 0) c it ed b y L in g (1 97 4) R U , N ov os ib ir sk 2 35 8 1 0. 28 - Z in ov je v (1 97 1) c it ed b y D an il ki n (1 99 9) R U , V ol ga 2 54 1 1. 85 - Ja za n (1 97 2) R U , L en in gr ad 2 3, 36 4 4 0. 12 - T im of ej ev a ( 19 74 ) R U , B ye lo ru ss ia 2a 19 0 3 1. 58 - K oz lo (1 98 3) R U , M ur m an sk 2 1, 20 9 1 0. 08 - M ak ar ov a (1 98 1) R U , A rk ha ng el 2 67 8 2 0. 29 - Fi lo no v (1 98 3) R U , V ol og da 2 2, 41 6 3 0. 12 - Fi lo no v (1 98 3) R U , T ve r 2 1, 72 6 1 0. 06 - Fi lo no v (1 98 3) R U , J ar os la vl 2 1, 31 2 2 0. 15 - Fi lo no v (1 98 3) R U , M os co w 2 2, 82 6 1 0. 04 - Fi lo no v (1 98 3) R U , K al ug a 2 62 7 2 0. 32 - Z ai ki n an d V or on in (1 98 6) c it ed b y D an il ki n (1 99 9) ALCES VOL. 39, 2003 NYGRÉN – MULTIPLE FECUNDITY IN MOOSE 91 R U , K ir ov 2a 32 7 3 0. 92 - G lu sh ko v (1 98 7) R U , K om i f ar m 4 23 0 1 0. 43 - K oz hu ho v (1 98 9) R U , C he rn oz em je 2 2, 04 0 2 0. 10 - Pr os ta ko v (1 99 6) c it ed b y D an il ki n (1 99 9) R U , K os tr om a fa rm 4 31 5 9 2. 86 1 V it ak ov a an d M in aj ev (2 00 0) B C , E st on ia 3 6, 72 1 60 0. 89 16 L in g (1 97 4) B C , E st on ia 2a 67 - - 1 K ir k an d T ön is so n (1 99 4) B C , E st on ia 1 - >4 - - K ir k an d T ön is so n (2 00 0) B C , E st on ia 2a 11 4 2 1. 75 - K irk (2 00 1) SC , S w ed en 2 - + - - L ön nb er g (1 92 3) SC , S w ed en 1 - 9 - 1 Sk un ck e (1 94 9) SC , F in la nd 2a 40 2 3 0. 75 - K oi vi st o an d R aj ak os ki (1 96 6) SC , N or w ay 1 - 2 - - L in g (1 97 4) 1 N A = N or th A m er ic a, R U = R us si a, B C = B al ti c C ou nt ri es , S C = F en no sc an di a. 2 1 = ra nd om o bs er va ti on s, 2 = f et us es , d et er m in ed b y hu nt er s, 2 a = fe tu se s, d et er m in ed b y sc ie nt is ts , 3 = c ow -c al f ob se rv at io ns , 4 = c al ve s bo rn o n m oo se f ar m s. 3 P re gn an t f em al es o r co w -c al f ob se rv at io ns . and also analyze triplet or quadruplet obser- vations or frequencies. The purpose of this paper is to: (1) report the frequency of multiple fecundity of moose in Finland from 1980 to 1999; (2) study the spatial and temporal variation of the frequency of multiple fecundity and the effects of environmental and geographical factors; (3) study the viability of litters with different numbers of progeny; (4) discuss the possible fecundity effects of selective harvest and evolutionary aspects of multi- ple fecundity; and (5) discuss possible dif- ferences in multiple fecundity of European and North American moose populations. STUDY AREA The study area was the whole of Fin- land. Finland mainly belongs to the boreal forest or taiga region, but is situated 500- 1,000 km further to the north than boreal forests elsewhere. In Fennoscandia, the vegetation is boreal but the light conditions are arctic (Solantie 2001). The typical vegetation types in Finland are coniferous forests (70%) and mires (30%). Approxi- mately 50% of the forests are pine (Pinus spp.) dominated, 30% spruce (Picea spp.) dominated, and 7% birch (Betula spp.) domi- nated. Since the 1950s, artificial forest regeneration with pine plantations through- out Finland has dramatically increased the amount of moose forage, but at the same time, it has restricted the distribution of other forage species. In Finland, all boreal vegetation zones are represented (Fig. 1). The bedrock of northern and eastern Finland (Lapland, Oulu, Kainuu, and Pohjois- Karjala) is mainly composed of ancient, nutrient-poor rock. The bedrock is more fertile in the southwestern part of Finland. The terrain of Finland is quite flat and the total area of lakes constitutes approximately 10% of the land surface. Due to the strong effect of the sea, the climate is moist. The winters are not as cold as in other boreal MULTIPLE FECUNDITY IN MOOSE – NYGRÉN ALCES VOL. 39, 2003 92 Northern boreal Middle boreal Southern boreal Hemiboreal Sweden Norway Russia Estonia Gulf o f Finlan d Gu lf o f B ot hn ia N Oroarctic Fig.1. Vegetation zones and Game management districts of the study area in Finland. areas. There are 110 snow-days per year in the hemi-boreal area and 200 days around the border of the central and northern boreal zones. The deepest snow layer (long-term average in March > 60 cm, 30-year maxi- mum 90-120 cm) and the mostly continental climate is typical for the districts of Pohjois- Karjala, Kainuu, Oulu, and Lapland where a small number of large predators exist and take their share of the moose population. In these areas (except Lapland), moose are the only numerous ungulate prey for brown bear (Ursus arctos) and wolf (Canis lupus). In coastal Finland, the seasons are less pro- nounced, the climate is more windy and humid, and the snow depth is lower (long- term average < 30 cm, 30-year maximum 60-80 cm). Data were collected in 15 game man- agement districts: Etelä-Häme (EH), Etelä- Savo (ES), Kainuu (KA), Keski-Suomi (KS), Kymi (KY), Lapland (LA), Oulu (OU), Pohjanmaa (PO), Pohjois-Häme (PH), Pohjois-Karjala (PK), Pohjois-Savo (PS), Ruotsinkielinen Pohjanmaa (RP), Satakunta (SK), Uusimaa (UM), and Varsinais-Suomi (VS). The districts were grouped into 4 regions: Coastal Finland (EH, KY, UM, VS, SK, and RP), Inland Finland (ES, KS, PH, PO, PK, and PS), Oulu (KA and OU), and Lapland (LA) (Figs. 1 and 2). The admin- istrative divisions of the data were based on the established practices of moose manage- ment in Finland. The division into regions was based on vegetation zones, the posi- tion/distance from the coastline, and com- parative calculations and long-term obser- vations of the spatial characteristics of the moose population (Nygrén and Pesonen, Finnish Game and Fisheries Research Insti- tute, unpublished data). In 1981-96, the estimated numbers in the winter moose population in the study area were between 67,000 and 93,000; the number of annual moose kills was between 26,000 and 69,000, and the average per- centage of kill in the total population was 39% (T. Nygrén and Pesonen 1989; Nygrén 1996; T. Nygrén, Finnish Game and Fisher- ies Research Institute, unpublished data). METHODS The Finnish Game and Fisheries Re- search Institute (FGFRI) collected data with the aid of Finnish hunters as part of the Finnish moose research program. The pro- gram has been conducted mainly for man- agement purposes since 1972. Two types of data and samples were used. R e p r o d u c t i v e O r g a n s o f P r e g n a n t Females The reproductive organs of female moose were collected during the hunting seasons of 1980, 1984, 1985, and 1989. In 1980 and 1985, the collection area was the whole of Finland (Fig. 2); in 1984, the sam- ples were collected from a 5,617-km2 area in the western part of the Oulu management ALCES VOL. 39, 2003 NYGRÉN – MULTIPLE FECUNDITY IN MOOSE 93 district and in 1989, from the Lapland game management district (Fig. 2). In 1980, 1985, and 1989, the moose kills in Coastal and Inland Finland were between 15 October and 15 December, and in Oulu and Lapland regions between 1 October and 15 Decem- ber. In 1984, the samples were collected during an exceptional winter hunt between 14 January and 31 January. Specimens of genitalia and jaws were also collected. The hunting teams were advised to take random samples from adult (> 1 year old) females and to send them as quickly as possible to the FGFRI Ilomantsi Game Research Sta- tion by mail. No preservative or freezing was used. In most cases, the material arrived in good condition within 1-4 days after the kill. The samples included ovaries, uteruses, vaginas, and, to determine age, jawbones or front teeth. Information about the date and place of kill, sex, carcass weight (weighed, estimated, or both), as well as information about lactation and pos- sible calves following or killed with the mother was included. The organ samples were studied and measured and the num- bers and measurements of the embryos/ fetuses were determined. All triplet and quadruplet cases were photographed. The ages of the females were determined by Matson’s Lab in Montana, USA, using ce- mentum annuli. The viability of single, twin, and triplet embryos were determined by comparing the embryo numbers with the numbers of single, twin, and triplet calves in the moose observation data. Moose Observations Since 1976, moose observations have formed the most important source of infor- mation for moose management in Finland. Each hunting day, the hunting teams clas- sify observed moose as bulls, cows without calves, cows with 1 calf, cows with 2 calves, or as unidentified animals. The teams are advised to record the observed animals on a card once a day, even if they were seen many times or by many hunters during the day. Usually, hunters give additional infor- mation if they have made an unusual obser- vation of triplet calves or killed some or all of them. When the hunting season is over, the teams mark the estimated number of moose still living in the hunting area on the observation card. The completed observa- tion card is sent to the Ilomantsi FGFRI by mail. In 1986-99, the average annual number of cards totaled about 4,300 and the aver- age number of moose observations exceeded 201,000. The average coverage of the returned cards was 83% (the coverage % is the proportion of licenses allowed to the hunting teams). The frequency of cows with 1, 2, or 3 calves was determined annu- ally and regionally from the observation data. In addition, the average weights of killed male and female triplet calves was determined and compared with the long- term average weights of killed moose calves 1980 and 1985 1980, 1984 and 1985 1980, 1985 and 1989 Sampling years 70 66 o 60 o o Fig.2. Sampling areas and regions of Finland used in the study. MULTIPLE FECUNDITY IN MOOSE – NYGRÉN ALCES VOL. 39, 2003 94 Table 2. Proportions of pregnant female moose (Alces alces) with 1-4 embryos in utero, collected from different areas of Finland between 1980 and 1989. Area/Year Number Number of embryos in utero of uteri 1 2 3 4 n % n % n % n % Coastal Finland 922 561 60.85 360 39.05 1 0.11 Inland Finland 931 510 54.78 417 44.79 4 0.43 Oulu 186 119 63.98 67 36.02 Lapland 308 227 73.70 80 25.97 1 0.33 1980 749 461 61.55 286 38.18 2 0.27 1984 67 49 73.13 18 26.87 1985 1,248 698 55.93 547 43.83 3 0.24 1989 283 209 73.85 73 25.80 1 0.35 Finland 1980-89 2,347 1,417 60.38 924 39.37 5 0.21 1 0.04 (Nygrén and Pesonen 1989). Additional information about unusually large litters was also given by mail or by phone to the Ilomantsi FGFRI. The reliabil- ity of this information was carefully checked before the results were included in the data set. Among them were reports about the triplet mother “Elli”, 3 sets of quadruplets, and a set of stillborn sextuplets. RESULTS Multiple Pregnancies in Finland In the data from 2,347 uteri of pregnant moose, 5 included triplets and 1 had quadru- plet embryos (Table 2). Four out of the five triplet sets were found in Inland Finland and one in Coastal Finland (Table 2, Fig. 3). The only quadruplet set was found in Lapland. Two triplet sets were recorded in 1980 and three triplet sets were recorded in 1985 (Table 2). No triplet or quadruplet sets were found in 1984 and 1989. Case studies of triplets and quadruplets: 1. An 8.5-year-old cow (EH 2267/80) was killed on 2 November 1980 (Fig. 3). The lengths of the embryos were 24 mm, 23 mm, and 24 mm, respectively. 2. An 8.5-year-old cow (KS 803/80) was killed on 16 November 1980 (Fig. 3). The embryo lengths were 82, 78, and 75 mm, respectively. Three primary yel- low bodies existed in the right ovary. 3. A 9.5-year-old cow (ES 4207/85) was killed on 15 October 1985 (Fig. 3). The cow had milk in its udder. The esti- mated carcass weight was 230 kg. The lengths of embryos were 4 mm; 3 pri- mary yellow bodies were found in the ovaries. 4. A 9.5-year-old cow (ES 2945/85) was killed on 20 October 1985 (Fig. 3). It did not have milk. The measured carcass weight was 175 kg. The embryo lengths were 16 mm, 6 mm, and 17 mm, respec- tively. One of the embryos had died before the cow was killed and its am- nion was twisted around the axis. All 3 primary yellow bodies were in the right ALCES VOL. 39, 2003 NYGRÉN – MULTIPLE FECUNDITY IN MOOSE 95 ovary. 5. A 12.5-year-old cow (PS 4961/85) was killed on 3 November 1985 (Fig. 3). It had milk and the estimated carcass weight was 215 kg. The embryo lengths were 13 mm, 11 mm, and 13 mm, re- spectively. Two embryos (13 and 11 mm) were in the left horn and one in the right horn (13 mm). The membranes in the left horn were tightly together. The membranes of the smaller embryo were twisted around the main axis, and the amount of fluid was small. The embryo itself seemed to be in good condition. Only 2 primary yellow bodies existed, both in the left ovary. Quite obviously, the embryos in the left horn were sin- gle-egg twins. 6. An un-aged cow (LA 958/89) was killed on 3 November 1989 (Fig. 3). The estimated dressed weight was 175 kg. The cow had milk and a male calf was following it (dressed weight 78 kg). The calf was killed just before its mother. The embryo lengths were 36 mm, 33 mm, 35 mm, and 34 mm, respectively. There were 2 primary yellow bodies in both ovaries. Triplet Observations in the Field The 585,149 calf-cow observations col- lected in 1986-99 included 191 triplet cows (0.033 %). The annual number of triplets varied between 1 (0.003%) and 28 (0.047%) (Table 3). The triplet degree correlated significantly with the twinning degree annu- ally (r = 0.605, df = 12, P = 0.022; Fig. 4) and an apparent 4-year cycle of twinning and triplet rate was found in 1988-99 when annual twin and triplet frequencies were compared (Fig. 5). In the game management districts, the triplet frequencies varied between 0.014% (Lapland) and 0.071% (Varsinais-Suomi) (Table 4). The frequencies were highest in Coastal Finland and decreased gradually to the North. The degree of twins and triplets was indicative of spatial correlation (r = 0.462, df = 13, P = 0.083; Fig. 6). An interesting case was the triplet mother “Elli” (Figs. 3 and 7). This moose cow, with a smaller than average head, was easy to identify. She was a yearling without Triplet calves Triplet embryos Quadruplet embryos Sextuplet calves Quadruplet calves “Elli”- the moose cow with five triplets Fig.3. Locations of multiple fecundity cases in Finland, 1980-2001. 34 35 36 37 38 39 40 41 42 0,00 0,01 0,02 0,03 0,04 0,05 % T R IP L E T S % TWINS Fig.4. Correlation of annual twin and triplet fre- quencies in Finland, 1986-99 (R = 0.605, df = 12, P = 0.022). MULTIPLE FECUNDITY IN MOOSE – NYGRÉN ALCES VOL. 39, 2003 96 Table 3. Annual proportions of single, twin, and triplet moose (Alces alces) cow-calf observations in Finland, 1986-99. Cows with Cows with Cows with Total cow-calf 1 calf 2 calves 3 calves observations Year n % n % n % n 1986 19,546 62.248 11,847 37.729 7 0.022 31,400 1987 21,412 61.761 13,256 38.236 1 0.003 34,669 1988 25,328 63.151 14,771 36.829 8 0.020 40,107 1989 28,334 63.580 16,218 36.393 12 0.027 44,564 1990 26,953 61.927 16,556 38.039 15 0.034 43,524 1991 25,226 59.993 16,806 39.969 16 0.038 42,048 1992 26,757 62.449 16,080 37.530 9 0.021 42,846 1993 28,939 63.971 16,282 35.992 17 0.038 45,238 1994 27,722 59.687 18,703 40.268 21 0.045 46,446 1995 25,678 63.826 14,541 36.144 12 0.030 40,231 1996 22,756 65.619 11,916 34.361 7 0.020 34,679 1997 21,559 60.371 14,135 39.582 17 0.048 35,711 1998 25,474 58.515 18,039 41.437 21 0.048 43,534 1999 35,890 59.665 24,235 40.289 28 0.047 60,153 Total 361,574 61.792 223,385 38.176 191 0.033 585,150 calves in 1989. During her life span “Elli” gave birth to 5 sets of triplets and 30 calves (Table 5). Because of a protection decision by hunters, only 6 of its offspring were killed as calves. “Elli's” family lived throughout the years in a territory of 1,200 ha. Often the family foraged in local gardens. If dis- turbed, “Elli” protected her calves with ex- ceptional violence. Almost all triplets were strong and similar-sized. The carcass weight of the single calf killed in 2000 was 114 kg - significantly over the 83 kg average carcasss weight of Finnish moose calves in the fall. In 1999, at the age of 11.5 years, “Elli” gave birth to her last triplet set. One of the calves, especially well-protected by the mother, was much smaller than the others were. In 2002 “Elli” gave birth to twins, was aging rapidly and limped with her hind leg. The last calf was born in 2003, probably prematurely, because the hunters never saw any calf that summer. “Elli” herself was finished at the age of 15 years on 14th July 2003 after the joint decision of hunters and scientists. She was very weak, carcass weight was 111 kg. Hardly any fat was found in her organs, but her teeth were in Fig.5. The 4-year cycle in twin and triplet fre- quencies in Finland, 1986-99. ALCES VOL. 39, 2003 NYGRÉN – MULTIPLE FECUNDITY IN MOOSE 97 good condition. Under the skin was found hundreds of lead pellets. One of the pellets had caused the chronic inflammation in the hip joint of the right leg. Also parasitic pneumonia was diagnosed and very high concentrations of cadmium were found in her liver and kidneys, but lead concentra- tions were low. Quadruplet Observations Four quadruplet observations have been documented in Finland: 1 in 1957 (Anon 1957) and 3 in 2000 (Fig. 3). In 1957, only 1 calf lived more than 1 week. In 2000, the Table 4. Proportions of single, twin, and triplet moose (Alces alces) cow-calf observations in different areas of Finland, 1986-99. Game management District/Area Cows with Cows with Cows with Total 1 calf 2 calves 3 calves cow-calf observations n % n % n % n Etelä-Häme 12,837 62.276 7,768 37.685 8 0.039 20,613 Kymi 19,401 62.083 11,830 37.856 19 0.061 31,250 Ruotsink. Pohjanmaa 17,249 58.680 12,139 41.296 7 0.024 29,395 Satakunta 20,056 60.966 12,831 39.004 10 0.030 32,897 Uusimaa 18,714 60.440 12,237 39.521 12 0.039 30,963 Varsinais-Suomi 17,729 57.063 13,318 42.866 22 0.071 31,069 Coastal Finland 105,986 60.155 70.123 39.800 78 0.044 176,187 Etelä-Savo 26,521 59.714 17,877 40.252 15 0.034 44,413 Keski-Suomi 31,225 60.838 20,074 39.112 26 0.051 51,325 Pohjanmaa 26,507 57.311 19,725 42.648 19 0.041 46,251 Pohjois-Häme 13,937 63.046 8,162 36.922 7 0.032 22,106 Pohjois-Karjala 21,992 63.126 12,840 36.856 6 0.017 34,838 Pohjois-Savo 25,566 56.351 19,793 43.627 10 0.022 45,369 Inland Finland 145,748 59.659 98,471 40.307 83 0.034 244,302 Kainuu 26,129 65.349 13,846 34.629 9 0.023 39,984 Oulu 47,498 64.861 25,719 35.120 14 0.019 73,231 Oulu 73,627 65.033 39,565 34.947 23 0.020 113,21 5 Lapland 36,213 70.390 15,226 29.596 7 0.014 51,446 Finland 361,574 61.792 223,385 38.176 191 0.033 585,150 28 30 32 34 36 38 40 42 44 0,01 0,02 0,03 0,04 0,05 0,06 0,07 0,08 % T R IP L E T S %TWINS Fig. 6. Correlation of twin and triplet frequencies in different areas of Finland, 1986-99 (R = 0.462, df = 13, P = 0.083). MULTIPLE FECUNDITY IN MOOSE – NYGRÉN ALCES VOL. 39, 2003 98 Fig.7. Moose female “Elli” with her triplet calves (photo: Vesa Mustonen 1995-96). Table 5. Annual calving history of “Elli”, a female moose (Alces alces) from Coastal Fin- land. Year “Elli’s” age Number of Number of (years) calves born calves killed 1988 0 0 1989 1 0 1990 2 2 2 1991 3 2 2 1992 4 2 1 1993 5 3 0 1994 6 2 0 1995 7 3 0 1996 8 3 0 1997 9 3 0 1998 10 2 0 1999 11 3 0 2000 12 1 1 2001 13 1 0 2002 14 2 0 2003 151 12 0 Total 30 6 1died 14th July. 2probably prematurely born, determined by inspection of “Elli's” genitalia. viability of 2 litters could be followed through the summer and in both cases only 3 of the 4 calves survived until the hunting season. In the third case, the quadruplet calves were observed for the first time in Septem- ber and no further observations were made during the hunting season. In three of the documented quadruplet cases, the size-difference of the calves was clear. In 1957, the total weights of the 3 dead quadruplets were 4.7, 7.0, and 9.5 kg. In 2000, one of the quadruplets was much smaller and weaker than the others were in 2 of the 3 observed cases of that year. Only the quadruplets observed in September were all of similar size but they were much smaller than average moose calves during that time of the year. Premature Birth of Sextuplets On 18 May 2001, a calving place of 6 premature moose calves was checked (Fig. 3). One stillborn calf lay at one end of the calving ground and 5 at the other end. According to the condition of the carcasses, the birth had taken place about 1 week earlier. The weights of the calves were 4.0 ALCES VOL. 39, 2003 NYGRÉN – MULTIPLE FECUNDITY IN MOOSE 99 kg (female), 3.8 kg (male), 3.5 kg (male), 3.3 kg (male), 2.7 kg (male), and 2.5 kg (female). The two smallest calves PK 1013/01 and PK 1014/01 (Fig. 8) had died some weeks earlier in the uterus. Vague signs of respiration were evident only in the male calf of 3.3 kg (PK 1012/01). Survival of Multiple Fetuses and Calves The proportion of early triplet embryo sets in the data was 0.21%, but the propor- tion of triplet calves observed in fall was only 0.03% (Fig. 9). According to this, the viability of triplet embryos is quite low. Only about 15% of triplet embryo sets seem to be complete up to the age of 6 months. The viability of quadruplets is probably even lower. Compared with the survival rate of tri- plet and quadruplet sets, the survival rate of single and twin embryos to the age of 6 months seems to be very high (Fig. 9). From the early embryonic period to the age of 6 months, the proportion of singles increased in the total data by 2.4%. The proportion of twin pairs decreased by 3.0%, while the proportions of triplet sets decreased by 85.5% and quadruplet sets by 100%. Con- secutively, from embryos in 1985 until calves in 1986, the figures were: singles +11.3%, twin pairs –13.9%, and triplet sets –90.8%. Multiple calves obviously have an insignifi- cant effect on calf productivity per fertile female (Table 6). Carcass Weights of Triplets The average carcass weight of triplets killed during the hunting period was 72.0 kg. The annual averages varied between 58.5 and 78.9 kg. For male triplets, the average weight was 74.9 kg (n = 62), and for female triplets 69.3 kg (n = 62). The carcass weights of female triplets varied between 37 and 100 kg and for male triplets between 41 and 106 kg. DISCUSSION Kozlo (1983) expressed strong doubt about the viability of triplet embryos. No definite evidence was available at the time that the triplet or quadruplet sets were ob- served to ensure they were the offspring of one moose female only. Later Kozhuhov (1989) as well as Vitakova and Minajev (2000) reported that in farming conditions, 9 viable triplet sets and 1 quadruplet set were Fig. 8. The stillborn sextuplets found on 18 May 2001 in Nurmes, Finland (photo: Tuire Nygrén). MULTIPLE FECUNDITY IN MOOSE – NYGRÉN ALCES VOL. 39, 2003 100 ovaries of the cow. Koivisto and Rajakoski (1966), Markgren (1969), as well as Kirk and Tõnisson (1999) have also reported cases of identical twins as a part of triplet embryo sets. Obviously monozygotic twins are a normal, but rare event, in the Euro- pean moose. In this study, 0.21% of the pregnant females had triplet embryos. About 20 years earlier, Koivisto and Rajakoski (1966) found 0.75% triplet embryos in the same area (n = 402). Heruvimov (1969) reported 1.42% triplet embryos in the Tambov region of Russia (n = 141), Kozlo (1983) 1.58% in Byelorussia (n = 190), and Kirk (2001) 1.75% in Estonia (n = 114). The frequen- cies of triplets in the former Soviet Union are often much higher than those observed in Finland. This is consistent with the find- ing that the frequency of triplets decreases towards the north (South and Central Rus- sia 0.28-1.69%, North Russia 0.04-0.22%) as reviewed by Danilov (1987). In the surveys based on the information provided by Russian hunters, the frequen- cies of triplet embryo sets varied from 0 to 1.72%. In reports with at least 1 triplet set observation, the average frequency of tri- plets was 0.14% (Table 1). Compared with the specialists´ results of embryo numbers, these lower frequencies were predictable. As, for example, Timofejeva (1974) has pointed out, the skills of the hunters seldom are good enough to reliably count the em- bryo numbers in the uteri during early fall. Fig.9. Proportions of single, twin, triplet, and quadruplet litters of embryos and calves in Finland. Table 6. Number of embryos per pregnant moose (Alces alces) cow and calves per calf-cow in Finland. Area n Embryos/pregnant cow n Calves/calf-cow Coastal Finland 922 1.39 176,190 1.40 Inland Finland 931 1.46 244,301 1.40 Oulu 186 1.36 113,215 1.35 Lapland 308 1.27 51,446 1.30 born. Most of the farmed triplets had, however, low birth weight and their death rate was high (Kozhuhov 1989). In this study, I have shown that multiple births also occur in nature and some triplet sets even survive until the next autumn. “Elli”, the 15 year-old cow moose, gave birth to 5 sets of triplets, 6 pairs of twins, and 3 single calves, and brought most of its 30 calves to adult- hood. On the Kostroma farm in Russia, one of the most productive moose females, “Alysha”, had given birth to triplets once at the age of 13 years (Kozhuhov 1989). Al- together, “Alysha” had been pregnant 14 times and given birth to 26 calves. The present material includes 1 triplet embryo set with only 2 yellow bodies in the ALCES VOL. 39, 2003 NYGRÉN – MULTIPLE FECUNDITY IN MOOSE 101 In most studied populations, the propor- tion of multiple fecundity cases has been zero but sometimes, in favorable conditions and/or in reports based on small sample sizes, the percentage of triplet embryos has been higher than 2%. In farming conditions, Vitakova and Minajev (2000) reported 2.20% triplets and 0.24% quadruplets (n = 409). Most probably, if all studied natural populations were included, the proportion of triplet embryo sets of European moose would vary between 0 and 1%. The overall percentage of triplet calf observations in fall was 0.03% in my mate- rial (n = 585,149). Twenty years earlier Koivisto (1963) reported not a single triplet cow in Finland (n = 39,818). Makarova (1969 cited by Ling 1974) reported 1 triplet set (0.40%) in the Moscow region (n = 248). Ling (1974) reported 60 cases of triplets (0.89%) in Estonia (n = 6,721). As expected, the triplet calf frequencies are lower than the triplet embryo frequencies. In the present material, triplet calf frequen- cies were highest in Southwest Finland and lowest in Lapland ( Table 3). This is also consistent with the earlier result that the number of multiple fecundity cases is less frequent in the North than in the South (Danilov 1987). The opportunities to compare the tem- poral change of multiple fecundity frequen- cies are very few. Koivisto and Rajakoski (1966) found 3 triplets (0.75%) in the uteri of 402 pregnant moose females. The twin- ning percentage was 49.8%. In this study, the proportion of triplet embryos was 0.21% and with twin embryos, it was 39.4%. How- ever, the proportion of twin calves in fall was lower in 1963-65 (24.7%) (Koivisto 1963) than in 1980-99 (38.2%). During 1963-65, all triplet sets and about 50% of twin pairs had been lost before the fall. In 1980-89, all of the quadruplet sets, 85% of the triplet sets, but only 3% of twin pairs, were lost from the population before the fall. The difference is considerable and hardly can be explained by the difference in methods. The most probable explanation is the differences of the age structure of fe- male populations. In 1963-65, the average age of harvested females was 3.3 years (n = 1,075) and only 6.3% of the killed females were > 7 years old (Koivisto, FGFRI, un- published). In the 1997-99 material (n = 2,584), the average age was 4.3 years and 19.5% of females were > 7 years old (Nygrén et al. 1999; T. Nygrén, FGFRI, unpublished). According to Glushkov (1987, 1991), the calves of older, experienced fe- males survive better than the calves of young females. Older females usually give birth earlier than younger ones and the earlier calves have a higher probability of surviving until or during the following winter (Ericsson and Wallin 1999, Keech et al. 2000). Ericsson and Wallin (1999) and Testa et al. (2000) found no significant difference in the survival rate of twin and single moose calves. My results, as well the results of Glushkov (1987, 1991), are the opposite, but according to Glushkov’s age-structured material (1987, 1991), the mortality rate of triplets, twins, and singletons in Northeast Russia was significantly higher than in Fin- land. All triplet sets and 82% of twin pairs were eliminated from the population before the first fall and the proportion of singletons increased by 8%. In the younger age classes (< 6 years), the elimination frequencies were higher than in the older age classes. Compared with Glushkov’s results (1987, 1991) and, for example, Osborne (1991) and Ballard et al. (1991), the viability prog- nosis for twin pairs (3% decrease in fre- quency) and singletons (2% increase in frequency) in Finland is high. A multitude of factors probably lie behind these differ- ences; at least the larger populations of large predators in Russia and North America as well the different age structure of MULTIPLE FECUNDITY IN MOOSE – NYGRÉN ALCES VOL. 39, 2003 102 populations explain some of the difference in calf survival. The average carcass weight of the har- vested triplets was 11 kg lower than the average overall carcass weight (83 kg) of moose calves in Finland (Nygrén and Pesonen 1989). The difference was 12.7 kg for female and 9.1 kg for male calves. At the time of birth, the normal weight of Finnish moose calves is about 8-13 kg (T. Nygrén, FGFRI, unpublished). Calves with a weight less than 7-8 kg are seldom viable (Heptner et al. 1966). This also seems to be the case in North America, where the maxi- mum fetal mass of a cow moose is, accord- ing to Geist (1974), nearly 23 kg. The upper limit of the total weight of the fetuses of European moose is unknown. However, if we assume that the total weight of normal twins is about 16-26 kg, we can calculate that a strong adult female could give birth to 3 viable 7 kg calves but for most females, 4 calves of this minimum size would be too much. At least this appeared to be the case with the observed quadruplet sets. None of these survived until the first fall. In 1957, only one survived; the dead calves weighed 4.7 kg, 7.0 kg, and 9.5 kg. According to the embryo numbers per pregnant female and the calf numbers per calf-rearing cow, the potential for repro- duction is highest in Inland Finland and lowest in Lapland. The differences in fe- male age structure (Nygrén 1999) can ex- plain most of the spatial productivity differ- ences existing; in the North, there are more young females without a calf than in the South, but in both areas, fertile females seem to be very capable to rear their calves to the first fall. In the North, no signs of higher calf losses were found. Knowing the harsh climate of the North, the result re- mains unexpected. Compared with the mortality of Russian and North American moose, the total natu- ral mortality of moose is low in Finland. Excluding hunting mortality, the average annual mortality of moose (both adults and calves) has been estimated at approximately 3% (T. Nygrén, FGFRI, unpublished). Usu- ally, only during severe winters with deep snow (> 1 m) and a dense moose population (4-8 moose/1,000 ha of land area) a few dead yearlings are found in Southern Fin- land in April-May. More regularly, dead calves and yearlings are found in Northern Finland, but even there the numbers are comparatively low. In Sweden, with sub- stantially higher moose densities than in Finland but with almost similar natural and hunting conditions, Cederlund and Sand (1991) estimated that the natural mortality of calves was no higher than 1%. The low death rate of moose calves in Finland also gained support from a helicopter survey conducted by Heikkinen (1998). He found that calves comprised 50.7% of the total number of moose in February-March 1998 in a 1,600 km2 sample area where the ob- served proportion of calves had been 48.4% two to three months earlier at the end of the hunting season in 1997 (T. Nygrén, FGFRI, unpublished). Obviously, the natural calf mortality of the present moose population of Finland is very low: the population of large predators is small, the amount and quality of forage is high, and, as a result of selective hunting, the population structure is very productive and the proportion of experi- enced females high. The triplet frequencies in Finland were highest in those areas with the highest calf production; the frequencies decreased to- wards east and north where the twinning degree has permanently been lower (Nygrén et al. 2000). The spatial correlation be- tween the twin and triplet frequencies was close to significant and the temporal corre- lation was significant. Earlier, Ling (1974) found a significant correlation between the frequencies of twins and triplets in Estonia. Later Kirk (2001) also reported high fre- ALCES VOL. 39, 2003 NYGRÉN – MULTIPLE FECUNDITY IN MOOSE 103 quencies of multiple pregnancies in Estonia. Ling’s survey methods (i.e., hunters’ ob- servations) have been criticized (e.g., Kozlo 1983) because the number of triplet and quadruplet observations was much higher than in all previous reports (Table 1). The main point raised by the critics was the possibility that orphan calves join with strange calf-rearing cows and thus cause false ob- servations of triplet or even quadruplet sets. However, moose research in Finland from 1971 to 1999 has not recorded a single case of moose females accepting orphan calves. On the contrary, there are numerous exam- ples of aggression rather than normal ago- nistic behavior between calf-cows and other moose (K. Nygrén, FGFRI, personal com- munication). Therefore, I find it quite pos- sible that Ling’s result (1974) was sound. The existing correlation between twin and triplet frequencies is consistent with the assumption that multiple fecundity is an extreme case of twinning. When the he- reditary potential for productivity is high, the age structure optimal, and the living conditions favorable for reproduction and survival, the frequencies of twinning and multiple fecundity cases tend to increase. The most important critical factors seem to be: (1) low population densities compared with the carrying capacity of the feeding grounds; (2) weak or nonexistent populations of large predators; (3) mild winter condi- tions and cool, humid summers; and (4) an age structure with a high frequency of females at their best reproductive age. All these factors existed in Finland during the survey. According to a theory by Geist (1974), cows conceiving twins or even triplets are favored in the rapidly expanding but slowly contracting moose habitats where forage is seasonally superabundant and the long day- light hours of the Northern summer permit carbohydrate accumulation and a greater rate of milk production. When resources are marginal, single calves are favored. Geist theorizes that there must be manda- tory selection for high reproductive rates in expanding populations of moose, favoring the evolution of twinning. He also thinks that under conditions of favorable forage availability and quality it can be expected that natural selection will act against cow moose bearing single calves, which can grow too large and chance dystocia. I have no record of such delivery difficulties as recorded for caribou (Bergerud, personal communication, according to Geist 1974) and find the selection against cow moose bearing single calves not very probable – not at least in Finnish circumstances. The living conditions are favorable. The heavily hunted populations are in a constant state of expansion (without any real increase in population numbers). The twin-rearing cows are better protected than the cows without calves and single-calf cows by legislation and selective hunting recommendations. As a result, the success of twin cows and twin and multiple calves to survive and repro- duce remains high, and the frequency of genes for higher reproductive potential can slowly increase. The number of multiple fecundity re- ports is much larger in the European than in the North American literature. There are several possible reasons behind the differ- ence. The first is the modern research methods, which seldom allow a sufficiently numerous sample size (Schwartz 1998). This could explain the small amount of multiple fecundity cases reported in North America. The second possible reason is a lower probability to make calf-cow obser- vations in North America, where hunting takes place closer to roads with smaller hunting teams. In Finland, big moose hunt- ing teams (Koskela and Nygrén 2002) use vast areas with a very dense road network. The third possibility is that the reported difference between multiple fecundity cases MULTIPLE FECUNDITY IN MOOSE – NYGRÉN ALCES VOL. 39, 2003 104 in Europe and North America is real, as has been speculated by Geist (1998). Perhaps the small number of multiple embryo and calf observations in North America is a result of a genetic difference in reproduc- tive potential compared to European moose populations. No direct evidence is available on the matter, but it would be unjustified to exclude the possibility of hereditary differ- ences in multiple fecundity between the area with 68 chromosomes (Gustavson and Sundt 1968) in Europe and the area with 70 chromosomes (Wurster and Benirscke 1967) to the east of Yenisei River in Russia and in North America (Boeskorov 1997). ACKNOWLEDGEMENTS This study was made possible by the work of tens of thousands of Finnish hunt- ers who annually aided with the samples, observations, and reports of moose during 1980-99. 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