Department of Ecological Sciences, Natural History Museum and Institute, Chiba ... Long-term monitoring of life-history traits and the effects of density upon them ...
Ecological Research (1997) 12, 111-118
Density effects on life-history traits of an island lizard population MASAMI HASEGAWA
Department of Ecological Sciences, Natural History Museum and Institute, Chiba, Chiba 260, Japan Long-term monitoring of life-history traits and the effects of density upon them were studied in an island population of the lizard Eumeces okadae. Although life-history traits such as clutch size, egg size and the proportion of mature reproductive females varied little over 7 years in the intact population, manipulation of density to simulate decreased population density enhanced juvenile growth rate, age at first reproduction, frequency of female reproduction and size-specific clutch mass. In particular, the proportion of mature females reproducing annually increased almost 10 times from 5.6% to 53.8% after the removal of some lizards. However, body size at first reproduction and egg size were almost identical under both high and low density conditions. This study suggests that there were strong density-dependent effects on several lifehistory traits and that E. okadae attained a density close to the carrying capacity of the environment. Key words: annual variation; density dependence; island population; life-history traits; lizard.
INTRODUCTION Lizards often attain an extraordinarily high density on islands where effective predators such as carnivorous mammals and snakes are absent or scarce (Case 1975, 1983; Case & Bolgar 1991; Hasegawa 1994a). Recent demographic analyses indicate that these high lizard densities are maintained mainly by low mortality rather than by high natality (Schoener & Schoener 1978, 1980, 1982; Hasegawa 1990). Under crowded conditions, lizards exhibit unique life-history characteristics such as small clutch size, delayed maturity and low frequency of egg production (Case 1983; Hasegawa 1994a). Parts of these life-history characteristics should be adaptive and genetically fixed traits in insular populations, while others might be environmentally induced under crowded, possibly resourcelimiting conditions. Comparative studies to detect a pattern in life-history traits exhibited by several insular populations are initially instructive (Case 1983; Hasegawa 1994a). However, these comparative field studies alone were unable to distinguish ecogenetic adaptive traits from environmentally induced ones, although temporal variations in lifeReceived 24 June 1996. Accepted 2 December 1996.
history traits in relation to population densities or climatic fluctuations are well known for lizards in general (Ballinger 1977; Dunham 1978, 1981; Abts 1987; Jones et dl. 1987). For a comprehensive understanding of life-history patterns, it is important to demonstrate which life-history traits show changes in phenotypes caused by a change in the environment (Seigel & Ford 1991; Stearns 1992; Ford & Seigel 1994). Eumeces okadae Stejneger, an endemic lizard of the Izu Islands, Japan (Hikida 1993), maintains an extraordinarily high population density on Miyakejima, where both snake and mammalian predators are absent (Hasegawa 1990, 1994a). This population has the demographic characteristics of high annual adult survivorship (> 75% in females and > 60% in males) and low natality, and has lifehistory characteristics of delayed maturity (3-4 years), smaller clutch size, larger egg size and biennial reproduction (Hasegawa 1984, 1990). Interisland comparison revealed that E. okadae matured earlier, and laid many small eggs annually on lowdensity islands where snake or mammalian predators were present. Analyses of prey abundance and diets suggested that E. okadae experienced low prey availability on high-density islands, probably due to exploitation and intraspecific competition (Hasegawa 1994a). In this study, it has been
112
M. Hasegawa
assumed that size at maturity and egg size are traits locally adjusted by natural selection, while variation in age at maturity, frequency of reproduction and clutch size are induced facultatively under a high population density. Because the Miyake-jima population ofE. okadae constantly maintained a high population density (ca 4000 ha -1) year after year before weasel introduction (Hasegawa 1990, 1994a), even a long-term study to monitor population consequences is not sufficient to evaluate how density influences lifehistory traits. In order to examine whether a high population density is responsible for biennial reproduction, delayed maturity and small clutch size, experimental manipulation of the population density needs to be first conducted. This study addresses identification of the traits which show phenotypic plasticity when population density is experimentally reduced. Specifically, lifehistory traits such as age at first reproduction, fiequency of female reproduction, clutch mass and egg size were selected for analysis. Before presenting the experimental results, annual variations in clutch size, egg size and proportion of reproductive females for an intact population were provided as base-line data of life history-traits.
METHODS Study site and fidd procedure This study was conducted on Miyake-jima (35~ 130~ 5514ha in area, summit 714 m a.s.1.), in the Izu Islands of central Japan. The islands were visited 41 times (1-9 days each) from August 1978 to August 1984. The study site was at an elevation of 40 m a.s.1, and 0.05 ha in area, and located near Miike port on the eastern corner of the island. In May 1981, the area was expanded to 0.08 ha. A detailed description of the study site is provided in Hasegawa (1984, 1990). Lizards were captured, marked by toe clipping, measured and released. Snout-vent length (SVL) and body mass were measured to the nearest 1 m m and 0.1 g, respectively. Males were considered to be mature if they had a well-developed hemipenis, ejaculated sperm and exhibited reddish nuptial coloration around their heads. Maturity and reproductive condition of females were determined after Hasegawa (1984). Briefly, if females were either
gravid or spent, they were classified as mature and reproductive in that year; otherwise they were classified as either immature or mature but non-reproductive. Since hatching was concentrated in late July-early August (Hasegawa 1984, 1985), juvenile cohorts were easily recognized by their SVL until their body sizes approached that of older age classes (usually 24 months after hatching; Hasegawa 1990). Therefore, lizards first marked before 24 months of age were precisely assigned to the year of hatching (cohorts). Annual variations were monitored for clutch size (1977-1983), egg size (1980-1983) and proportion of reproductive females (1978-1983) for females captured at various localities on the island (altitude below 150 m a.s.1.). Clutch size was determined by counting yolked follicles larger than 4 m m in diameter and oviductal eggs for the dissected specimens, and for eggs found in the natural nests or those laid in the laboratory. In order to obtain data on egg size, a total of 37 gravid females (4-15 females year-1) were captured and brought back to the laboratory. After measuring live mass and SVL, females were reared individually in plastic containers with damp peat moss and small flat stones for nesting sites. These containers were placed in a dark room, and the room temperature was kept at approximately 25~ Containers were checked daily until the start of egg laying. Within 12 h of egg laying, the body mass of spent females and individual eggs were measured to the nearest 1 mg.
Demonstration of density effects Density effects on life-history traits were examined by an experimental density manipulation at the Miike study site. To simulate an increase in adult mortality, large-sized individuals including adult males and non-reproductive females were removed during the period from July 1981 to July 1983 (Table 1). The lizards removed from the Miike site were released at the opposite side of the island about 6 km away. Hatchlings, yearlings and gravid or post-reproductive females were left in order to examine whether these unremoved individuals exhibited enhanced growth and reproduction. Because topographic conditions surrounding the study site did not allow for the designation of suitable control sites, life-history traits were compared for the lizards collected before and during the
Density effects on lizard life-history
113
Table 1 Removalprotocol ofEumeces okadae from a study site at Miike, Miyake-jima 1981 Number captured Hatchlings and yearlings 2-year-olds and adults Number removed 2-year-olds and adults % lizards removed Biomass removed (g)
1982
11-19 July
12 August
16-19 April
11 May
29 24
41 22
47 51
44 34
19 8
180 139
31 31.6 306.3
25 32.1 225.7
5 18.5 48.7
94 29.5 930.1
24 45.3 250.3
9 14.3 99.1
removal experiment. It was assumed that the observed demography of the study plot during experimental treatment would have remained the same as it was in the years before manipulation if the density had not been altered. This was a reasonable assumption, as considerable climatic fluctuations that might have been responsible for annual variation in life-history traits had not been experienced in the area (see Results). Any differences between years must therefore result not from gross climatic change but from manipulation. The number of lizards living in the Miike study site was estimated from recapture data primarily during the summer months. Population size was estimated by a small-sample Lincoln Index method (Bailey 1952). The biomass of given cohorts was determined by multiplying the population size and mean body mass of the lizards belonging to the respective cohorts. Age and size at first reproduction, growth rates of juveniles, reproductive frequency of females and clutch mass were compared between the years before (1978-early 1981) and the years after experimental density reduction (late 1981-1983). Age and size at first reproduction and frequency of female reproduction can be determined directly through recapturing lizards whose previous reproductive conditions were known. Growth rates of juvenile lizards were calculated by dividing the increment in SVL by the number of days between the first and subsequent measurements. Clutch mass was indirectly estimated for individual females. Because the body mass of gravid females changed little from the mating season (April-May) to just prior to egg laying (M. Hasegawa, unpubl, data), body mass in the mating season minus body mass in the spent condition can approximate clutch mass. By this procedure, clutch mass of individually marked females
9 July
Total
was estimated. In April-May 1982, six gravid females were captured from an experimental site and their egg masses (see above for laboratory procedure) were compared with those captured in other years at various localities within the islands.
RESULTS Annual variation in life-history traits During the course of this study (1978-1983), annual precipitation varied'from 2508 to 4107 mm (Fig. 1). Weather conditions were relatively stable, but the summers of 1981-1983 were slightly cloudier (a total of 464.3-582.7 sunshine hours during July-September) than those of 1978-1980 (454.4-672.8 hours). Annual variations in clutch size, egg mass and proportion of reproductive females are shown in
10000
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"~ 1000 ' r
100 1974
9
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1976
,
~
1978
.
i
1980
'
i
1982
.
.
19'84
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.
19~86 19'88
19'90
Year
Fig. 1. Variation in the annual total (--O--) and summer (July-September) subtotal (--O--) rainfall on Miyake-jima from 1975 to 1988. The horizontal solid bar indicates the period of the present study.
114
M. Hasegawa
Fig. 2. The mean clutch sizes varied from 7.2 to 8.4 (Fig. 2a),. but the difference between the years was not statistically significant (F6,162 = 1.278, P> 0.10). For the samples in which both female SVL and clutch size were known, an ANCOVA was performed for the log-transformed clutch size with log-SVL as a covariate. The result of this analysis indicated that the clutch size adjusted by SVL did not vary annually (Fs,104= 0.819, P > 0.05) from 1978 to 1983. Egg mass was essentially independent of maternal SVL (r= 0.113, P> 0.50, n = 37), and did not differ significantly between the years (Fig. 2b; F3,33 = 0.900, P> 0.45). The proportion of reproductive females (no. reproductive females/ no. mature females) varied little from year to year (Fig. 2c; X2= 2.99, P > 0.05). Approximately 50% of the mature females were reproductive each year.
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Density effects During the period from July 1981 to July 1982, a total of 94 large lizards amounting to 930 g in fresh mass were removed from the study site (Table 1). This treatment corresponded to a removal of about 1200 adult lizards per ha (94 0.08 ha-1) or a biomass of 11.6 kg haq. The estimated density of adult lizards concomitantly decreased from an average of 2500 ha-1 (1978-1980) to 990 ha -1 (1981-1983; Table 2). This amount of density change (decrease of about 1500 lizards ha-1) nearly equaled the number of lizards removed. The estimated biomass of adult lizards decreased from an average of 25.3 kg haq (1978-1980) to 9.3kg haq (1981-1983; Table 2).
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Age at first reproduction The manipulation of adult density elicited predicted responses in the life-history traits (Table 3). Although no yearling lizards were reproductive either before or after density manipulation, more 2and 3-year old lizards became reproductive after density manipulation (Table 3). The proportion of 2-year-old lizards that became reproductive significantly increased from 0% to 15.0% for females (Fisher's exact probability test, P < 0.05) and from 15.5% to 71.4% for males (X2 = 27.28, P< 0.001). The proportion of 3-year-old lizards that became reproductive also increased but was not statistically significant (Table 3).
(c)
(d)
" n .............[ ] .............[] ...........
65
1976 19t77 19'78 19'79 19'80 19'81 19'82 19'83 19~84 Year
Fig. 2. Annual variations in the life-history traits of female Eumeces o/eadae: (a) clutch size; (b) egg size; (c) proportion of mature femalesreproductive each year; and (d) the smallest body size (SVL) of the newly mature Eumeces okadae. Circles and squares represent females and males, respectively. Open symbols indicate the values obtained from the control years (1978-1980) and the surrounding undisturbed sites (1981-1983), and solid symbols indicate values obtained from the experimentalyears (1981-1983). Vertical bars indicate SD above and below the mean (O) for the clutch (a) and egg (b) sizes. Numerals above each value indicate sample sizes.
Density effects o n lizard life-history Table 2
115
Population size, density and biomass of a Eumeces okadae population at Miike, Miyake-jima in August Population size
Yearlings 1978 1979 1980 1981" x control year 1982" 1983" x experimental
St
nt + 1
11 13 23 29
23 12 32 14
18 11 year
2-year-olds and adults 1978 30 1979 38 1980 51 x control year 1981" 13 1982" 39 1983" 17 x experimental year
mt + 1
Mean
SD
5 4 4 3
44.0 33.8 151.8 108.8
4.3 3.0 11.9 7.7
37 27
6 3
97.7 77.0
7.4 9.6
37 39 20
9 10 8
114.0 138.2 119.0
5.4 5.5 4.0
21 11 16
5 4 2
47.7 93.6 96.3
4.3 4.7 10.6
Biomass (g ha ~)
Density (no. ha-1)
Body mass (g)
880 676 3036 1359 1488 1221 963 1092
5.62 5.19 5.57 5.51 5.47 4.79 5.44 5.12
4946 3508 16 911 7490 8142 5851 5236 5543
2280 2764 2380 2475 596 1170 1204 990
11.72 8.66 10.58 10.32 8.21 9.27 10.03 9.17
26 722 23 933 25 180 25 278 4892 10 846 12 078 9272
*Study site was expanded to 0.08 ha. St, number of lizards marked and released at time 1; n t + 1, number of lizards captured at time t + 1; m t + 1, number of marked lizards captured at time t + 1.
after removal (Table 4). G r o w t h rates o f newly hatched lizards from August to O c t o b e r and those o f yearling lizards from April to August did not increase even after removal (0.217 m m vs 0.171 m m for hatchling, and 0.172 m m vs 0.126 m m for yearling, respectively). O n the contrary, the mean growth rates from August to O c t o b e r increased significantly from 0.074 m m (n = 18) in the years before removal ( 1 9 7 8 - 1 9 8 0 ) to 0.132 m m (n = 21) in the years after removal ( 1 9 8 1 - 1 9 8 2 ; two-tailed >test, P < 0.001). D u e to enhanced growth during
In spite o f the decrease in age at first reproduction in both sexes, m i n i m u m mature size did not decrease correspondingly. T h e smallest SVL o f newly matured lizards varied little each year in both males ( 6 9 - 7 4 m m ) and females ( 7 2 - 7 7 m m ; Fig. 2d), and the smallest third o f newly matured lizards did not differ significantly in SVL between the years before and after removal (Mann W h i t n e y U-test, P > 0.2 for males,/9 > 0.5 for females). G r o w t h rate in SVL (ram day -z) was compared for juvenile lizards between the years before and
Table 3
Summary of the effects of population removals on the life-history traits of Eumeces okadae
Life-history traits % Mature at 2 years of age Male Female % Mature at 3 years of age Male Female Minimum s v L at maturity Male Female Frequency of reproduction % breeding annually
Control 1978-1981 Mean n
Experimental 1982-1983 Mean n
Significance level
12.5% 0.0%
64 55
71.4% 15.0%
P < 0.001 P < 0.05
93.5% 62.5%
31 32
100.0% 100.0%
69-74 mm 73-76 mm
SVL, snout-vent length; NS, not significant.
5.6%
21 20 7 5
69-72 mm 71-77 mm 18
53.8%
NS NS NS NS
13
P < 0.01
116 Table 4
M. Hasegawa Comparison of growth rate in SVL (mm day-1) of juvenile Eumeces okadae before and after density manipulation
Cohort
Control year Mean SD n
Hatchling (Aug.-Oct.) 1980
0.217
0.011
0.164 0.181 0.162 0.174 0.048 0.080 0.091 0.074
Yearling (Apr.-Aug.) 1979 1980 1981 Pooled Yearling (Aug.-Oct.) 1978 1979 1980 Pooled
Cohort
Experimental year Mean SD n
Significance level
5
1981
0.171
0.029
7
1 16 8 25
1982
0.126
0.031
12
0.031 0.025 0.027
0.126
0.031
12
0.016 0.034 0.026 0.032
5 8 5 18
1981 1982
0.135 0.127
0.030 0.028
13 8
0.132
0.029
21
P < 0.05
NS
P < 0.05
NS, not significant.
summer, particularly in 1981, the yearling lizards attained an SVL (72.7 mm _+ 3.9 SD) larger than minimum mature size (ca 70 ram) at the end of the second growing season. These growth data indicated that an earlier age at first reproduction after removal was due to enhanced growth of the yearlings, especially during summer, and not due to reduced body size at maturity.
Clutch frequency The reproductive performance of 31 reproductive females was followed for at least 2 successive years before and after density manipulation. Before removal, only one of 18 females classified as reproductive in the preceding years was detected to be reproductive in the following years, whereas after removal, seven of 13 females became reproductive in 2 successive years. This increase in frequency of female reproduction from 5.6% to 53.8% was statistically significant (one-tailed Chi-squared test, Z 2 = 9.21, P < 0.005).
S V L (.t71,27 = 0.016, P < 0.05) for the two groups, showing that females laid clutches heavier than before. The mean mass of eggs laid by females captured at the study site in May 1982 (594 mg, n = 6) did not differ significantly from those laid at other localities in other years (568-621 mg, n = 21; twotailed Mann Whitney U-test, P > 0.05). Increased clutch mass but not individual egg mass after removal suggested an increase in the number of eggs per clutch. Before removal, adjusted mean clutch masses at an SVL of 82 mm (mean female SVL; Hasegawa 1994a) were 3.1-3.6g. Clutch mass divided by egg mass (574 mg) will yield an estimated clutch size of 5.4-6.1. After removal, adjusted clutch mass increased to 4.5-5.1 g which yielded an estimated clutch size of 7.7-8.7. 1.0 0.8
i
Clutch and egg mass Clutch mass of females captured in the years after removal were compared with those in the years before removal (Fig. 3). A one-way ANCOVAwas performed on the estimated clutch mass with SVL as the covariate. Both clutch mass and SVL were transformed to logarithmic values (base 10). This analysis revealed a significant difference in the adjusted mean clutch mass (F1,28 = 6.84, P < 0.05), but not in the slopes of the regression of clutch mass on
0.6
~ 0.4 (O O.E 0.0 1.86
o
0 o
i
l
i
i
I
1.88
1.90
1.92
1,94
1.96
log SVL
Fig. 3. The effect of experimental density reduction on the size-specific clutch mass of Eumeces o/eadae. (2), values obtained from the control years; 0 , values obtained from the experimental years.
Density effects on lizard life-history DISCUSSION
This study is an experimental approach to examine how density affects the life-history traits of lizards normally living under an extraordinarily crowded condition. Before discussing density effects on lifehistory traits, the possibility that changes in lifehistory traits are due to natural annual variation should be ruled out. Due to a rich and stable amount of annual precipitation on Miyake-jima, it was unlikely that variation in precipitation (e.g. primary production) influenced the life-history traits of the lizards via variability in food supply as frequently demonstrated for several desert systems (Ballinger 1977; Dunham 1978, 1981; Abts 1987). In the temperate regions with relatively rich rainfall on the other hand, the amount of sunshine hours is considered an important environmental factor influencing the growth and reproduction of lizards (Jones et al. 1987). Slightly cloudier weather conditions in 1981-1983 than in 1978-1980 would cause a delay in age at first reproduction and a decrease in frequency of female reproduction if the magnitude of fluctuation was sufficient to induce annual variation in the life-history traits. However, clutch size, egg mass and proportion of mature reproductive females did not differ between the years, at least in the intact population, suggesting that the climatic fluctuation during 1978-1983 was not large enough to induce annual changes in a subset of life-history traits that were selected or that these life-history traits were insensitive to climatic fluctuation. Therefore, age at first reproduction and clutch frequency at the study site would also have remained the same during experimental treatments, had density not been altered, and any differences in the life-history traits at the study site between the years must result from experimental density manipulation. The present study demonstrated that, when density was reduced artificially, both males and females became reproductive at earlier ages, females laid larger clutches and about 50% of the mature females reproduced in 2 successive years. These short-term responses i n life-history traits should be a typical ease of phenotypic plasticity, whereas egg size and minimum body size at first reproduction were almost identical between the high and low
117
density conditions. Rigorous analysis of factors affecting phenotypic plasticity was unable to be conducted in the field due to uncontrolled changes in either prey availability or unspecified environmental factors. Nevertheless, the results summarized above are very similar to the results of laboratory experiments by Siegel and Ford (1991) and Ford and Siegel (1994). They demonstrated that clutch size, clutch mass and age at maturity of an oviparous snake were most subject to plasticity, while egg size and minimum size at first reproduction were almost identical between the low and high diet feeding groups. They suggested that offspring size may reflect actual adaptive differences among populations. This study demonstrated that a factor affecting phenotypic plasticity in the life-history traits of E. okadae was population density. When density was experimentally reduced, the unremoved members of the population would be allowed to acquire more food resources for growth and reproduction, or reduced interactions would allow the lizards to conserve energy otherwise expended for intraspecific interactions. In the former case, reduction of population density would increase overall prey abundance by reducing prey consumption. Several recent field studies demonstrated that lizards were capable of depleting prey abundance particularly in insular environments (Pecala & Roughgarden 1984; Schoener & Spiller 1987; Spiller & Schoener 1988; Lewis 1989). In the latter case of intraspecific competition, the competitive effect is a simple function of population density independent of prey abundance. As population density decreases, interactions among individuals simply decrease. Although my field experiment was not initially designed to evaluate the relative importance of exploitative and interference types of competition, both seem to be equally important. Because E. okadae did not have any fixed feeding territories and certain areas were shared by at least 100 individual lizards on Miyake-jima (Hasegawa 1994b), not only resource depletion but also interferences to foraging activities would occur. The life-history consequences of the removal experiment (Table 3), therefore, support the idea that growth and reproduction are limited by high population density probably very close to the carrying capacity of the environment.
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ACKNOWLEDGEMENTS I thank E Hayashi, H. Higuchi, T. Hasegawa, Y. Kigasawa, Y. Matsumoto for their help during the field work and for K. Miyashita for his continuous encouragement during the study. Thanks are also due T. Kusano for critically reading the manuscript.
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