Effect of Temperature on Development, Survival, Oviposition, and Diapause in ... Total fecundity is highest at 21·C. In the laboratory, most adults live beyond.
Effect of Temperature on Development, Survival, Oviposition, and Diapause in Laboratory Populations of Sepedon juscipennis (Diptera: Sciomyzidae)1 JEFFREY K. BARNES Department of Entomology, Cornell University, Ithaca, NY 14853 ABSTRACT
Sepedon fuscipennis Loew was reared in the laboratory under constant temperature regimes to determine the effect of temperature on several life history features. Develop· mental and oviposition rates are greatest at 30°C. Total survival of the immature stages is greatest at 33°C. The intrinsic rate of increase is positive over the 15-33°C range, and it peaks at 30·C where rm 0.137 day·'. Adult longevity increases as temperature decreases. Total fecundity is highest at 21·C. In the laboratory, most adults live beyond the age at which they contribute significantly to the intrinsic rate of increase. S. fuscipennis is a typical polyvoltine species exhibiting imaginal facultative diapause. Diapause is characterized by cessation of ovarian development, cessation of spermatogenesis, and hypertrophy of fat bodies. Both temperature and photoperiod influence diapause induction in the sensitive and responsive adult stage.
=
Since Berg (1953) first suggested that malacophagy may be a widespread habit among larvae of the family Sciomyzidae (marsh flies), knowledge of the fundamental life histories of these flies has expanded considerably. Most reared species feed upon aquatic or terrestrial snails, but a few are known to attack slugs (Trelka and Foote 1970) or fingernail clams (Foote 1976). Larvae that attack aquatic snails, including larvae of some species of Sepedon, are overt predators, killing and consuming several snails before they pupate. Sepedon juscipennis Loew occurs throughout most of the United States and Canada. Adults typically occur among the vegetation of swamps and marshes, along the shorelines of lakes and ponds, and in the vegetation along the edges of slow-flowing streams. They breed continuously throughout life, and several overlapping generations are produced each year. Females usually oviposit a few centimeters from the water surface on stems and leaves of aquatic or semiaquatic plants. They place the eggs side by side in orderly rows containing variable numbers of eggs. After eclosion the larvae fall into the water and float just beneath the surface film. They are effective swimmers, and this may increase their chances of encountering snails, which they kill and consume more or less quickly depending upon the size of the prey. Larvae kill almost any species of pulmonate snail they encounter, and the number killed depends upon the density of the snail populations (Eckblad 1973, 1976) and the sizes of the snails. Pupae, encased in puparia, float freely just beneath the water surface (Neff and Berg 1966). Several recent studies deal with the predator-prey relationships and population ecology of sciomyzid flies and snails. These studies have been stimulated primarily by an interest in evaluating the effectiveness 1 Part of a thesis submitted in 1975 to the faculty of the Graduate School, Cornell University, in partial fulfillment of the requirements for the M.S. degree. This investigation was supported by Research Grants GB-329l7X and BMS75-10451 from the General Ecology Program, National Science Foundation, and by Cooperative Agreement No. 12-14-1001-400 between' the Agric. Res. Serv., USDA, and the Dept. of Entomol., Cornell Univ. Received for publication Dec. 23, 1975.
of sciomyzid larvae as possible biological control agents of snail hosts of trematode diseases such as schistosomiasis and fascioliasis (Berg 1964, 1973). Geckler (1971) studied snail predation by Sepedon tenuicornis Cresson in the laboratory to determine the number of snails killed per larva, the time required to make the first kill, and the vulnerability of snails as a function of predator and prey size. Eckblad and Berg (1972) studied the dynamics of a natural population of Sepedon fuscipennis Loew in Ithaca, New York, and Eckblad (1973) experimentally manipulated populations of S. fuscipennis and pulmonate snails in the laboratory and in the field to determine the effects of predator and prey densi. ties, prey aggregation, and water depth on the num· ber of snails killed by each larva. All of these studies deal with species of the genus Sepedon because they are easily identified, relatively easily reared, and common and conspicuous throughout much of North America (Neff and Berg 1966). This study is an attempt to determine the effect of temperature on certain life history features of S. fuscipennis, including fecundity, developmental rates, and longevity. This type of information facilitates evaluation of beneficial species and their climatic limitations (Birch 1948, Mackauer and van den Bosch 1973, Messenger 1964), and it aids in defining optimal laboratory rearing conditions. Materials and Methods Collection Sites Laboratory-reared progeny of adults collected in July and August, 1974, were used in studies of fecundity and adult longevity. They were collected by sweeping stands of Sparganium eurycarpum Engelman along the west shore of Dryden Lake, 3.2 km SE of the village of Dryden, Tompkins Co., NY. Progeny of adults collected during the summer of 1975 were used in all other laboratory studies. They were collected from stands of Phalaris arundinacea L. in Bull Pasture Pond on the Cornell University Golf Course, Ithaca, Tompkins County.
1089
1090
ENVIRONMENTAL ENTOMOLOGY
Rearing Techniques Laboratory rea rings were kept in incubators at desired temperatures ±O.5°C. The relative humidity within each incubator was maintained above 70%. Unless otherwise indicated, a LD 16: 8 lighting schedule was used for all rearings. Adults were held in clear plastic vials (4.7 cm X 10.6 cm) fitted with screen caps. A layer of moist cotton was packed onto the bottom of each vial to maintain high humidity. A wooden medical applicator stick provided a resting site for the flies. The artificial diet consisted of 10 parts honey, 9 parts casein hydrolysate, and 6 parts nutritional yeast. A pea-size mass of this food was placed on the wall of each rearing vial, and a crushed snail was placed on the moist cotton. The artificial diet and the water used to moisten the cotton contained 0.1 % Tegosept M®" as a mold inhibitor. Flies were transferred to fresh vials weekly at temperatures below 26°C and semi-weekly at higher temperatures. The cotton and applicator sticks were removed after counting the eggs, which were usually laid on the walls of the rearing vials. Enough water was added to cover the bottom of each vial. The vials were then packed into transparent molded plastic boxes and held in incubators until the eggs hatched. The humidity in the boxes was above 95 % at all experimental temperatures. Rearings of 1st instars were initiated in Stender dishes (1.9 cm X 4.4 cm) containing about 5 mm of water. It was often difficult to obtain large numbers of small snails as food for the larvae, but it was found that 1st instars feed equally well on large snails that have been crushed. Depending upon their availability, either live Lymnaea or live Physa were offered to second and third instars. Biomphalaria glabrata (Say), which is easily reared in the laboratory, was used to maintain non-experimental fly cultures during the winter when it was difficult to collect local species. Enough snail tissue was always available in all rearings to meet the demands of the growing larvae. If several larvae were reared together they were transferred early in the 2nd stadium to larger molded plastic boxes (13.2 cm X 18.5 cm X 10.5 cm [w X 1 X h)) containing about 5 mm of water. Larvae were transferred by means of a camel's hair brush to fresh rearing containers, and the food supply was renewed every 12 h at temperatures above 21°C. At lower temperatures this procedure was carried out every 24 h. Immediately after pupariation (Fraenkel and Bhaskaran 1973) puparia were transferred to individual 21 mm X 70 mm glass vials containing a layer of moist cotton. The vials were plugged with dry cottO::1 and placed in incubators to await emergence of adults. Experimental Procedures Male-female pairs of progeny of the flies collected at Dryden Lake in 1974 were kept in individual rearing vials. Dates of emergence, first oviposition, and • Inolex Corporation,
Philadelphia. PA.
Vol. 5, no. 6
death were recorded for each individual. If the male of a pair died before the female, it was replaced. The number of eggs laid by each female and the sizes of egg rows were recorded whenever the flies were transferred to fresh vials. Adult females collected in June and July, 1975, provided the eggs used in all estimates of egg developmental times and survival. About 30 females were placed in each incubator, and eggs from the first few days of oviposition were discarded. At most experimental temperatures eggs were harvested at one-hour intervals and observed at one-hour intervals for eclosion until the number hatching every hour was very low. At 10 and IS °C eggs were harvested and observed at 12-h intervals. Egg survival was estimated by calculating the proportion of eggs that hatched in each of several replicates at each temperature. One replicate consisted of several eggs, usually more than 30, laid by an acclimated female over a period of 2-3 days. At each experimental temperature 7 cohorts were initiated, each consisting of 50 first instars that hatched during the previous 12 hours. Each cohort was observed every 12 h, and the number of larvae alive, the number that molted, and the number that pupariated were recorded. The number that molted was estimated by counting all cast larval integuments recovered. The period from pupariation to emergence of the adult was also estimated by observing puparia every 12 hours. This period includes the prepupal period of Fraenkel and Bhaskaran (1973). The term puparial period has been adopted for the purposes of this study. Dissections to determine the condition of internal genitalia were made in Ringer's solution at 12X magnification under a binocular dissecting microscope. Measurements were made at SOX magnification with an ocular micrometer calibrated to the nearest 0.01 mm. Squash mounts of spermathecae and testes were examined under a phase-contrast microscope to determine the presence or absence of sperm. Statistical Analysis Standard statistical methods, as outlined in Snedecor and Cochran (1967), were used throughout this study. Logarithmic transformations were found to stabilize the variance in several comparisons, and geometric means are reported in such cases. Student's t-test was used in comparisons of two means, and Scheffe's test was used in comparisons of more than two. Results Fecundity Females usually oviposit in the laboratory from a few days after emergence until death. Rarely is a period of more than 2 or 3 days passed in which a given female lays no eggs. Total fecundity is quite variable among females at any particular temperature. In general, longer-lived females lay more eggs than short-lived females. Fecundity is maximal in
December 1976
BARNES:
LABORATORY
Table I.-Oviposition
POPULATIONS
1091
Sepedon juscipennis
OF
data for Sepedon IU8cipenni8 at constant temperatures,"
Fecundity (eggs'female-l)
Oviposition rate (eggs'day-')
Egg row sizeb (eggs'row-l)
Temp. (DC)
n
Mean'
C.V.
Max.
Mean"
C.V.
Max.
Mean
C.V.
Max.
15 21 26 30 33
17 59 54 52 24
125.5 321.2 304.3 236.8 57.3
16.3 19.2 19.5 23.2 30.0
374 1801 2129 1180 374
3.0 6.3 9.6 12.5 5.8
51.7 33.4 36.3 45.7 75.2
9.4 17.3 33.0 41.7 20.8
5.5 6.6 5.1 5.0 3.7
32.4 32.9 34.2 37.3 46.9
9.2 14.0 11.3 10.6 8.5
" Females that did not oviposit are excluded from this analysis. b Calculated from average egg row sizes for individual females.
('Geometric means.
the 21-26DC range and falls off abruptly below 21 DC and above 30·C (Table 1). The maximum number of eggs laid by any female was 2129. Oviposition Rates Rates of egg-laying for individual females during short periods may reach 50 or more eggs/day. Sustained rates of 25 or 30 eggs per day are not uncommon in the 10-30·C range. Average rates of egg-laying were calculated by dividing the total num-
ber of eggs a female laid by the length, in days, of the oviposition period. A rapid, almost linear, increase in the mean oviposition rate occurs between 15 and 30·C, but between 30 and 33·C it falls abruptly (Table 1). Figure 1 illustrates the day-to-day oviposition rates for 5 cohorts held under various constant temperatures. The plotted fecundity values, designated by m"" are the numbers of female eggs produced per female of age x per day, assuming a sex ratio of 1: 1.
.30 .It.'1
"""'"I
.'5 .• 0 I• •15
.10
.05
62
10.
B'
142
~22
16'
18.
47
'7
67
B7
107
.47
"7
167
187
207
.27
13 .40
12
26°
.,,,
.35
30°
33°
11
,,-.j
10
.30
.25 7
I.
m•
•20
B
.15
•• 0
-.
-
•05
19
J9
59
79
......
._MM.__ .._____ ~._.._._.. 99
119
139
159
179
17
57
77
17
37
57
(da,sl
Age
FIG. 1.--Survivorship (1" dotted line) and fecundity constant temperatures.
37
(m"
solid line) curves for Sepedon fuscipennis
at various
1092
Vol. 5, no. 6
ENVIRONMENTAL ENTOMOLOGY
Table 2.-Preoviposition periods of Sepedon luscipennis at constant temperatures.
Temp. (·C)
15
18
21
54
n
19
13
Mean" (days)
3~6
1~2
C.Y.
14.3
9~
6.7 20.2
26 57
30
49
7A
5A
19.9 21.5
33 25 9S
15.3
" Geometric means.
In all cases, oviposition reached a high and sustained rate rapidly. There is some evidence of a gradual fall in the rate as the flies reached the age of maximum longevity. This pattern is commonly observed in insects, and it has been reported for other Sciomyzidae (Beaver 1973). The graphs for 15, 26 and 30·C show a sudden increase after the gradual decline. This is due to oviposition by a small number of very long-lived individuals. Egg Row Size The egg rows produced by a single female vary considerably in size, from one to 30 or more eggs/ row. The average egg row size was calculated for each female by dividing the total number of eggs she laid by the number of rows. The unweighted means of these values indicate that egg row size is also influenced by temperature (Table 1). The largest egg rows are produced at 21 ·C, and those at higher temperatures are consistently smaller. Egg rows collected in the field are similar in size to, or slightly larger than, those produced in the laboratory. Field-collected females ovipositing in the laboratory consistently produce larger egg rows. Nine females collected from Bull Pasture Pond and allowed to oviposit in the laboratory for 2 days produced rows of mean size 12.1±1.0 eggs (mean± SE) . A 2nd group, consisting of 18 females that were allowed to oviposit for 5 days in the laboratory, produced rows of mean size 13.3±1.2 eggs. It was not uncommon to find egg rows consisting of as many as 40 or more eggs laid by field-collected flies in the laboratory. Such large rows almost never result from oviposition by laboratory-reared females, not even by individual females over short periods. Development and Survival of Adults Female Sepedon fuscipennis do not oviposit im-
mediately after emerging from their pup.aria. The duration of the preoviposition period vanes greatly with temperature, and the minimum in this study o~curred at 30°C (Table 2). At 33°e the preovlposltion period is considerably longer. As the temperature decreases below 300e the preoviposition period increases. Adult longevity, the period from emergence from the puparium to death, decreases greatly as temperature increases (Table 3). No significant differences were found between male and female mean longevities (P > 0.10). Survivorship curves for females are shown in Fig. 1. The proportion of females alive at the beginning of an age interval of pivotal age x days is designated by Ix. The familiar reverse-sigmoid shape of these curves has been termed a "wearing-out" pattern (Cole 1954). The survival.of newly emerged adults is fairly high, but as the files grow older, survival drops. At most temperatures a majority of adult death occurs during a distinct age period around the mean, and a few members of the population seem to have much greater ability to survive than others. Maximum longevity is, in general, 2-3 times greater than the mean (Table 3). Development and Survival of Immature Stages The egg, larval, and pupal developmental periods (Table 4) follow a pattern similar to that described for the preoviposition period. The shortest periods occur at 30·e, except for the puparial period which is still shorter at 33 ·C. The increased periods above 300C are statistically significant for eggs and larvae through the 2nd stadium (P < 0.05). The larval periods listed in Table 4 are for development from eclosion to the end of the ] st, 2nd, and 3rd stadia. The durations of the 2nd and 3rd stadia may be estimated by taking the differences of the appropriate means. At all temperatures above ] O°C the 2nd stadium is the shortest by 80-50 hours. The ] st and 3rd stadia are of approximately equal duration. No differences were noted between male and female puparial periods. The developmental periods may be converted to rates by taking their reciprocals. When plotted against temperature, the developmental rates describe a roughly sigmoid curve. These curves have been simulated for eggs, larvae, and pupae by using a sigmoid function with the relationship inverted above
Table 3.-Longevity of adult Sepedon Juscipennis at constant temperatures.
Males Temp.
Females
(·C)
n
Mean" (days)
C.Y.
Max.
n
Mean" (days)
C.Y.
Max.
15 21 26 30 33
20 57 57 50 43
83.3 64.7 35.8 27.7 19.2
14.1 18.7 16.1 17.8 18.2
195 164 98 72 38
22 67 55 55 40
73.8 53.9 39.6 23.2 16.7
lOA 24.5 15.0 24.4 20.1
124 199 170 72 37
" Geometric means.
December 1976
BARNES: LABORATORY POPULATIONS OF
Table 4.-Mean temperatures .•
18 21 26 28.5 30 32 33
at constant
Larvab
(oC)
15
1093
developmental periods in hours for immature stages of Sepedon luscipennis
Temp. 10
Sepedon fuscipennis
Egg
I
I & II
I,II & III
Pupa"
431.4 (7.5,314) 307.1 (1.3,193) 172.9 (0.5,222) 105.3 (0.5,409) 81.4 (0.5,289) 72.1 (0.5, 192) 65.9 (0.6,205) 67.5 (0.6,144) 67.9 (0.6, 160)
402.9 (1.8, 48) 288.8 (1.9, 97) 144.5 (2.7, 145) 127.8 (2.9,188) 84.7 (2.9, 195)
810.8 ( 1.4, 5) 528.4 (1.4, 50) 271.0 (1.7,127) 230.7 (1.7, 140) 151.2 (2.0, 159)
1235.9 (0.2, 2) 776.2 (0.7, 33) 427.7 (1.3, 99) 343.9 (1.2, 115) 237.9 (1.8,147)
ND 400.3 (1.4, 28) 293.9 (0.7, 90) 191.0 (0.8, 101) 145.0 (0.9,131)
77.0 (4.0,199)
137.6 (2.4,151)
214.4 (2.0, 120)
118.5 (1.1,110)
74.3 (4.4,200)
139.5 (2.1,165)
224.2 (1.9,161)
114.7 (1.4,105)
• Geometric means are reported. Numbers in parentheses are coefficients of variation of logarithmically transformed data and numbers of individuals on which the means are based, respectively. b I, II and III designate developmental periods from eclosion to the end of the 1st, 2nd and 3rd larval stages, respectively. "Includes both pupal and prepupal developmental periods.
the temperature corresponding to the maximum developmental rate (Stinner et al. 1974). The formula for this function is as follows: where RT = rate of development at temperature T,
C = asymptote of the curve, k1;k2 = empirical constants, '{T,forT~toPt an d T 2.topt-T, for T > topt' topt temperature at which the maximum developmental rate occurs.
=
Parameter estimates are given in Table 5, and the functions are plotted in Fig. 2-4. Survival of immature stages, the proportion of individuals entering one life stage that survive to the succeeding life stage, is also temperature-dependent. The egg survival data presented in Table 6 indicate that at ~30°C, less than 10% mortality occurs in most cases. Survival is reduced considerably at 33°C. The survival of several hundred eggs laid at room temperature by 23 ~ and held at 34.5°C was QI ClI 0
,079 .218 .288 .370 .294 .171
The ~uparia were mis-
",-.-----1---------.--15
20
25
30
Temperature (OC J FIG. 4.-Developmental rates of Sepedan fuscipennis pupae. Rates were calculated by taking the reciprocal of the developmental time, Solid lines represent fitted sigmoid functions with parameter estimates as given in Table 5.
December 1976
BARNES: LABORATORY POPULATIONS OF
mortality (A.M.) and real Table 7.-Apparent mortality (R.M.) of Sepedon luscipennis larvae at constant temperatures. First instars
Second instars
Third instars
Temp. (OC)
A.M.
R.M.
A.M.
R.M.
A.M.
R.M.
10 15 18 21 26 30 33
.769 .489 .317 .257 .243 .267 .251
.769 .539 .432 .384 .419 .408 .470
.753 .659 .385 .377 .309 .302 .196
.174 .372 .359 .419 .403 .338 .275
1.000 .460 .364 .285 .197 .324 .226
.057 .088 .209 .197 .178 .254 .255
------
perature and incubated at 2-4°C beginning on the 5th day after pupariation, only 8 yielded healthy adults when warmed to 20 e (Stephen L. Arnold, unpubl.). A few adults that attempted to emerge died before escaping from the puparia; a few that did emerge did not live longer than a few hours. Neff and Berg (1966) found that pupa ria collected in the field during the winter invariably fail to yield adults. 0
Intrinsic Rate of Increase The method of computing the intrinsic rate of increase, rl/l' from tables giving age-specific survivorship (/J') and fecundity (lnJ.) values is thoroughly discussed in Birch (1948, 1953) and Andrewartha and Birch (1954). In this study the values of were estimated by iteratively solving the equation :::'I.,.m".exp( -rlllx) = ]. The results from 5 laboratory populations are given in Table 8. The intrinsic rate of increase is greatest at 30°C, and it declines rapidly above and below this temperature. It becomes negativc bctwecn 10 and 15°C because no viable pupae are formed at 10°C. It also becomes negative somewhere above 34.5°C because very few eggs hatch at this temperature. The net reproduction rate, Ro, is greatest at 26°C, and the mean generation time, T, and doubling time are shortest at 30°C. rill
Diapause This and other studies have confirmed a rapid population decline (Eckblad and Berg 1972) and an initiation of diapause in Sepedon fuscipennis by late August in the Ithaca, New York, area. Of 16 Cj1
1095
Sepedon fuscipennis
collected at Dryden Lake in late August 1973, and held at 2] °C and LD ]5:9, only 2 oviposited by January. Of 35 Cj1 collected at Dryden Lake in early September 1973, and held at 25°e and LD 17:7 only one oviposited within 2 wk, but 14 oviposited by the end of September and 29 oviposited by the beginning of November. The onset of diapause appears to be influenced by both temperature and photoperiod. More than 30% (n = 22 and 32) of the females reared at 15 and 18°C under a LD 16:8 lighting schedule did not lay eggs within the usual range of preoviposition periods . At 21, 26, and 30°C, fewer than 4 Cj1 (n = 52 to 63) did not oviposit. Dissections of 6 nonovipositing females held at ] 8 °C revealed that the ovaries and accessory glands were not well developed, and fat hypertrophy was apparent. However, dissections of 12 o held at 18°C revealed well-developed testes and no fat hypertrophy. Mature sperm were present in all of these males. Forty-nine percent (n = 37) of the females that were reared at 30°C and LD 16: 8, and transferred to 21°e and LD 8: 16 within 12 h after emergence, oviposited, but only 26% (n =42) of those reared at 21°C and LD 16: 8 oviposited after transferal. Several females were reared at 2] and 26°C under LD 8:16. One oviposited at 21°C (n = 21) and one at 26°C (n = ]3) within 40 days. Thirty female pupae were collected from Bull Pasture Pond in late June, 1975. They emerged in the laboratory at 21°C and LD 8:] 6, and only 13% oviposited. Apparently the freshly emerged adult female is sensitive to the factors that initiate diapause. If egg, larval, and pupal stages are passed under longday conditions, but the freshly emerged adult is maintained under short-day conditions, diapause incidence is high. However, this does not rule out the possibility that the conditions to which the immature stages are subjected in some way moderate diapause incidence or intensity in the adult. The proportions of ovipositing female S. fuscipennis were smaller in groups reared through the entire life cycle under LD 8: 16 than in groups transferred from long-day to short-day conditions at about the time of adult emergence. It also appears that an adult that has begun to oviposit is not sensitive to diapause induction by short-day conditions. Casual observations never revealed arrest of oviposition by a previously
Table B.-The intrinsic rate of increase and related statistics for populations of Sepedon. fuscipen.nis constant temperatures.
Temp. (0C)
15 21 26 30 33
r••
R. (Cj1
Cj1 / Cj1 )
4.1 74.0 86.7 62.6 5.7
• The age at which ~Ixmxexp(-rmx)
(Cj1
Cj1 / Cj1 /day)
0.013 0.076 0.117 0.137 0.057 = 0.95.
A (Cj1
.
(=e''') VVday)
T (days)
Doubling time (days)
(days)
1.013 1.079 1.124 1.146 1.059
108.6 56.3 38.3 30.3 30.4
53.3 9.3 5.9 5.1 12.1
137.2 63.3 44.0 35.1 36.5
XO.95
at
1096
ENVIRONMENTAL
Vol. 5, no. 6
ENTOMOLOGY
hypertrophy of fat bodies in both sexes (Lees 1955, Stoffolano and Matthysse 1967). These characteristics are found in diapausing S. juscipennis. Dissections of males and nonreproducing females that were held at 21 DC and LD 8: 16 for several weeks usually revealed that the fat bodies were well developed compared with those of reproducing individuals. Also, ovaries, testes and accessory glands are larger in nondiapausing than in diapausing, laboratory-reared S. juscipennis (Fig. 5). Only 6 of the 15 J flies held at 21 DC and LD 8: 16 for several weeks after emergence had any mature sperm in their testes. Most of these 6 J had very few sperm compared with flies held at LD 16: 8, and the diapausing females paired with them had no sperm in their spermathecae. Discussion
FIG. 5.-Dorsal view of dissections of abdomens of male (top) and female (bottom) Sepedon fuscipennis. Fat hypertrophy and reduced size of testes, ovaries and accessory glands are apparent in diapausing flies (left) when compared with nondiapausing flies (right). Arrows indicate 1 mm.
ovipositing female after transferal to LD 8: 16. This problem requires further work, however. Oviposition is slowed or even stopped by low temperatures, but it is not known whether diapause is induced in the mature adult. In the laboratory, diapause in S. juscipennis is easily terminated by transferring flies to relatively high temperatures and long photoperiods. Several females were maintained in a nonreproductive condition at 21 DC and LD 8: 16 for 3-5 weeks. All of the 9 ~ that were then transferred to 300C and LD ] 6: 8 oviposited within 2 wk, whereas only 4 of the 21 transferred to 300C and LD 8: 16 oviposited. Five of the 9 ~ transferred to 21 DC and LD 16: 8 oviposited within a month, but none of the 26 transferred to 21 DC and LD 12: 12 oviposited before the experiment was ended 4 wk later. It is not known whether females that have been in diapause for longer periods or at colder temperatures can be induced to oviposit by simply raising the temperature and lengthening the photoperiod. Imaginal facultative diapause in insects is usually characterized by cessation of ovarian development in females, cessation of spermatogenesis in males, and
All species must evolve certain minimal values of their rates of population increase to overcome environmental resistance and to compete successfully with other species. Higher rates of increase may confer no advantage, because resultant increases in intraspecific competition and depletion of resources can be disastrous. Inasmuch as oviposition, survival, and developmental rates determine the potential rate of increase, a species can attain the optimal rate of increase in several ways. The effect of the life history and ecology of a species on the rate of increase can be better understood by analyzing the relative contributions of these 3 variables and by considering the effects of environmental fluctuations. A population's capacity for increase is inversely related to the mean generation time, T, and variation in T has much more effect on the capacity for increase than variation in the net reproduction rate, Ro' The developmental time for all immature stages of S. juscipennis accounts for more than half of the mean generation time at all constant temperatures for which calculations have been made in this study, so reductions in developmental times for this species can have a significant impact on the potential rate of population increase. This study has also shown that the intrinsic rate of increase is positive over a wide range of temperatures, but it and the developmental rates for all immature stages are maximal at about 30 C, well above average summer temperatures in the Ithaca, NY area. Several features of S. fuscipennis ecology may enable the various life stages to take advantage of microenvironmental elevations of temperature. Adults are found among unshaded emergent vegetation where they may move between sunlit and shaded sides of stems and leaves to help regulate their body temperature. Adult pigmentation may play a role in the thermoregulation of some Sciomyzidae (Zuska and Berg 1974). S. fuscipennis eggs are also found on stems and leaves of exposed vegetation. Larvae and pupae are confined to the area just below the water surface where temperatures are often higher than elsewhere in a body of water. It is possible to estimate the degree to which survival of immature stages affects the rates of increase of laboratory populations of Sepedon fuscipennis D
December 1976
BARNES:
LABORATORY
POPULATIONS
under constant temperature regimes. In the follow· ing discussion the capacity for increase, ro (In;:;IJ.In,,,) T" .,, is used instead of the intrinsic rate of increase, r"" because any alteration in Ro causes both r", and T to change, whereas Te, the mean generation time associated with re' remains constant (Laughlin 1965). This constant relationship simpliflies the argument for the purposes of illustration. If I; is defined as the proportion of emerging adults that are still alive at age x, and if no death of immature stages occurs, then the capacity for increase is given by the formula r~ (ln~/;m:J) Te·'. But if only a proportion, Ii' of the eggs laid eventually result in emerging adults, the capacity for increase is given by the formula r" = (In"J:.I;l;.In,,,) Te·'; re is lower than r;' by the amount -(inl;) Te·'. Estimates of r;'-r,. are presented in Table 9. The reduction in the capacity for increase because of mortality of immature stages becomes greater at higher temperatures. Much of this effect is due to the shorter generation times at higher temperatures. However, the percentage by which the capacity for increase could be augmented by eliminating the mortality of immature stages is smallest at 26°C and increases as temperature decreases or increases. This is reasonable because sur· vival of the immature stages is greatest at 26°C and decreases as temperature decreases or increases. The values of and the corresponding population doubling times are also presented in Table 9. In the range from 15-33°C the larval stage has the greatest influence on total survival of immature stages of S. fuscipennis. Egg and pupal survival values are above 0.9 in most cases, so mortality during each of these stages is reducing the capacity for increase by less than -(In 0.9)Te·' = 0.0028 day·' at 26·C. On the other hand, larval mortality at 26·C reduces the capacity for increase by 0.0227 day·'; the influence of larval mortality is around an order of magnitude greater than that of egg or pupal mortality. It is also possible to make an intuitive evalu· ation of the relative importance of adult mortality. The age at which 95% of the value of rIll is ac· counted for is estimated by finding an age XO.nr; at which ;:;l.,.m.,.exp(-r",x) = 0.95. Table 8 shows these values for the 5 temperature regimes used in this study. By locating these ages on the appropriate adult survivorship curves (Fig. I) it is seen that, in most cases, adult mortality is low during the age
=
=
r;
OF Sepedon
1097
fuscipennis
intervals in which they make the greatest contribution to the intrinsic rate of increase. In other words, adult mortality is also of relatively minor significance compared with larval mortality. Variations in the factors that influence larval survival may play a major role in determining the rate of increase in natural populations. In the laboratory, apparent mortality of 1st instars is not markedly greater than apparent mortality of 2nd or 3rd instars, but some evidence indicates that it is greater in the field. First instars can successfully attack only a limited size range of snails (Beaver 1972, Geckler 1971). Allowing a cohort of 1st instars to feed once before releasing them in the field increases totallarvaJ survival several fold over that of a cohort that is not fed prior to release (Eckblad and Berg 1972). Lar· val survival is significantly influenced by snail densities and water depth (Eckblad 1973). When the water is deep, snails have a much larger available habitat per unit surface area, whereas the larvae are restricted to the surface. Oviposition rates follow the same pattern with respect to temperature as developmental rates and survival of immatures; they are high at 300C, and they decrease as temperature increases or decreases. These 3 factors determine the rate of population increase. The strong concordance with respect to temperature results in a high rate of increase at 30·C. Comparison of oviposition rates (Table 1), developmental rates (Table 4), and survival rates (Table 6) gives an intuitive feeling for the relative contribution made by each factor to the intrinsic rate of increase (Table 8). The decreased oviposition and survival rates appear to be the predominant factors in determining the intrinsic rate of increase at 33·C because developmental rates decrease only slightly at this tempera· ture. Between 30 and 21 ·C, differences in the oviposition and developmental rates apparently have a predominant role. Below 21·C all 3 factors are im· portant. Longevity and total fecundity do not follow the same pattern with respect to temperature as the 3 factors listed above. Longevity and fecundity do not contribute greatly to the intrinsic rate of increase, as long as they are above certain limits. Females beyond age Xo.nr, do not contribute significantly to the intrinsic rate of increase, but many females live long beyond that age in the laboratory (Fig. I). Most fe-
TabJe 9.-The hypotheticaJ capacity for increase resulting from elimination of mortality in the immature stages of Sepedon !uscipennis at constant tcmperatures. --
---
--._-
--
---~-----
Temp.
~-~---~--
------
With mortality of immatures
Without mortality of immatures
(OC)
r,
Doubling time (days)
r;
Doubling time (days)
r;-rc
15 21 26 30 33
0.013 0.050 0.083 0.123 0.056
54.6 13.8 8.3 5.6 12.3
0.036 0.065 0.102 0.159 0.114
19.5 10.7 6.8 4.4 6.1
0.023 0.Q15 0.019 0.036 0.058
(r;-rc)rc•'·l00%
179.5 29.0 22.2 29.6 102.3
1098
ENVIRONMENTAL ENTOMOLOGY
males beyond age XO.\l5 continue to oviposit at high rates for a considerable period. Reproduction by these older females is probably of considerable value in helping the population get through periods when standing water is absent from the habitat and periods of low snail densities. The seasonal cycle of S. fuscipennis is similar to that found in many polyvoItine species. The time of the year in which food is plentiful and climatic conditions are favorable is used for reproduction. The number of generations each year probably depends to a great extent on the sum of the effective temperatures. This study has shown that diapause is facultative, and it is induced in the sensitive and responsive adult stage by short daily photoperiods and low temperatures, but prevented by long photoperiods and high temperatures. Diapause is also characterized by cessation of ovarian development, cessation of spermatogenesis, and hypertrophy of fat bodies.
Acknowledgment I am indebted to Professor Clifford O. Berg for his encouragement and advice throughout this study. Drs. R. G. Helgesen and J. G. Franclemont also contributed helpful suggestions and criticisms. Stephen L. Arnold critically reviewed the manuscript. REFERENCES
CITED
Andrewartha, H. G., and L. C. Bircb. 1954. The Distribution and Abundance of Animals. University of Chicago Press, Chicago. Beaver, O. 1972. Notes on the biology of some British sciomyzid flies (Diptera: Sciomyzidae). II. Tribe Tetanocerini. Entomologist 105: 284-99. 1973. Egg laying studies on some British sciomyzid flies (Diptera: Sciomyzidae). Hydrobiologia 4:\: 1-12. Berg, C. O. 1953. Sciomyzid larvae (Diptera) that feed on snails. 1. Parasitol. 34: 630-6. 1964. Snail control in trematode diseases: the possible value of sciomyzid larvae, snail-killing Diptera. Pages 259-309 in B. Dawes, ed. Advances in Parasitology, Vo!. 2. Academic Press, London and New York. 1973. Biological control of snail-borne diseases: a review. Exp. Parasitol. 33: 318-30. Birch, L. C. 1948. The intrinsic rate of natural increase of an insect population. J. Anim. Ecol. 17: 15-26. 1953. Experimental background to the study of distribution and abundance of insects. I. The influence of temperature, moisture, and food on the innate capacity for increase of three grain beetles. Ecology 34: 698-711.
Vol. 5, no. 6
Cole, L. C. 1954. The population consequences of life history phenomena. Quart. Rev. BioI. 29: 103-37. Eckblad, J. W. 1973. Experimental predation studies of malacophagous larvae of Sepedan juscipenllis (Diptera: Sciomyzidae) and aquatic snails. Exp. Parasito!. 33: 331-42. 1976. Biomass and energy transfer by a specialized predator of aquatic snails. Freshwater BioI. 6: 19-21. Eckblad, J. W., and C. O. Berg. 1972. Population dynamics of Sepedan juscipennis (Diptera: Sciomyzidae). Can. Entomo!. 104: 1735-42. Foote, B. A. 1976. Biology and larval feeding habits of three species of Renacera (Diptera: Sciomyzidae) that prey on fingernail clams (Mollusca: Sphaeriidae). Ann. Entomol. Soc. Am. 69: 121-33. Fraenkel, G., and G. Bhaskaran. 1973. Pupariation and pupation in cyc\orrhaphous flies (Diptera): terminology and interpretation. Ibid. 66: 418-22. Geckler, R. P. 1971. Laboratory studies of predation of snails by larvae of the marsh fly, Sepedan tenuicarnis (Diptera: Sciomyzidae). Can. Entomol. 103: 638-49. Laughlin, R. 1965. Capacity for increase: a useful population statistic. J. Anim. Ecol. 34: 77-91. Lees, A. D. 1955. The Physiology of Diapause in Arthropods. Cambridge University Press. Mackauer, M., and R. van den Bosch. 1973. General applicability of evaluation results. Pages 330-335 in R. D. Hughes, ed. Quantitative evaluation of natural enemy effectiveness. 1. Appl. Ecol. 10:
321-51. Messenger, P. S. 1964. Use of life tables in a bioclimatic study of an experimental aphid-braconid wasp host-parasite system. Ecology 45: 119-31. Neff, S. E., and C. O. Berg. 1966. Biology and immature stages of malacophagous Diptera of the genus Sepedoll (Sciomyzidae). Bull. Va. Agric. Exp. Stn. 566: 1-113. Snedecor, G. W., and W. G. Cochran. 1967. Statistical Methods, 6th ed. Iowa State University Press, Ames, Iowa. Stinner, R. E., A. P. Gutierrez, and G. D. Butler, Jr. 1974. An algorithm for temperature-dependent growth rate simulation. Can. Entomol. 106: 519-24. Stoffolano, J. G., Jr., and J. G. Matthysse. 1967. Influence of photoperiod and temperature on diapause in the face fly, Musca autumna/is (Diptera: Muscidae). Ann. Entomol. Soc. Am. 60: 1242-6. Trelka, D. G., and B. A. Foote. 1970. Biology of slug-killing Tetanacera (Diptera: Sciomyzidae) . Ibid. 63: 877-95. Zuska, J., and C. O. Berg. 1974. A revision of the South American genus Tetanaceroides (Diptera: Sciomyzidae), with notes on colour variations correlated with mean temperatures. Trans. Roy. Entomol. Soc. Lond. 125: 329-62.
