MINI REVIEW
PERIODICITY AND DIVERSITY IN ANT MATING FLIGHTS ELW~D
S. MCCLUSKEY
Physiology Department, Loma Linda University, tama Linda, CA 92350, USA. (Received 2 March 1992; accepted 1 April 1992) Abshwt-1.
Plight hours and seasons are alike within species, but differ among species and among
genera. 2. Laboratory studies indicate internal circadian control of the phase relation to the light-dark cycle, with field evidence for modiition by temperature (or other environmental variables). 3. In at least two species there is abrupt loss of obvious rhythm after mating, suggesting some special function before loss, e.g. to facilitate cross-breeding within species or reproductive isolation between
t~RoDu~oN Noteworthy features of the mating system in ants include the special castes involved, the elaborate means for cross-colony synchronization within a species, and the enormous diversity within the family [see Hiilldobler and Wilson (1990) for a comprehensive account]. In many species the winged sexual castes are produced at a certain season. Mating occurs during or following a flight at a characteristic time of day, when males encounter females from other colonies. The inseminated females then start new colonies. This brief review of both published and unpublished studies wilf examine two main questions: how diverse are the flight times among species and genera? and what controls their timing? HOW TAXONOMICALLY DIVERSE ARETHE FLIGHT TIMES? l%e Aights of the colonies of a particular species in a given area are typically at the same time of day
and season (Talbot, 1945; Kannowski, 1963): e.g. Prenalepis imparis, early spring in the warmest part of the day (Talbot, 1945); Solenopsis maniosa, early summer in late afternoon before sunset (McCluskey and McCluskey, 1984). The same phenomenon is illustrated by four species of Pago~arn~rrne~~ all in the same season and locality: colonies of any one species fly at the same hour, but different species at different hours (Hiilldobler, 1976). Not only are flight times more alike within than among species; they are also more alike within than among genera (McCluskey, 1973, 1974, 1982; MacKay and Ma&Lay, 1984). The best illustration of this is from the George Reserve in Michigan, where Paul Kannowski and especially Mary Talbot studied numerous mating flights (at least 34 species, in nine genera), all in one locality. Thus, variability associated with multiple localities is greatly reduced,
increasing the validity of comparison of the ants themselves. When their flight records (largely cited in McCluskey, 1973, 1974) are plotted hour against season (McCluskey, in preparation), the species of each one of the six genera with more than one species are clearly grouped; and on average, each genus overlaps only one of the others. The same pattern is illustrated by flights which were not only all in one locality (Tucuman, Argentina) but also on the same day (Kusnezov, 1962). Of the 15 genera with good flight records, only two had enough species for a good comparison. All four Wenopsis species were flying in the late morning, but no Pfteidole; and all nine PheSole species at the end of the day, but no Sokopsis (compiled from Kusnezov). WHAT CONTROLS THE TYMlNG? Relationship to temperature
Records from the George Reserve were again used, but only those with morning Bights, so as to avoid the complications due to afternoon reversal of temperature. In each one of the six species with enough flights to compare different days (four species of Formica, two of Dolichoderus) the tiights were later the cooler the day (McCluskey, in preparation). But there are limits to such a relationship. For example, if Messar andrei do not fly before the nest is exposed to the sun, they do not fly that day at all (McCluskey, 1963). The same is true for colonies of N. pergandei around Colton, California, if a certain temperature is not reached soon after the nest is exposed to the sun, and of Pogonomyrmex cafifornict~s if they do not fly by noon (McCluskey, unpubtblished). It is as if there were a “time window”, within which flight is affected by temperature or other factors. Consistent with this conclusion is the finding that both hour and temperature seem necessary to explain the diversity of timing of field worker ant
ELWOODS. MCCLUSKEY
242
0
0
12
6
18
24
houw
Fig. I. Rhythmof male and female fIight in constant temperature. Winged Fogonomyrmex californicus (a red harvester ant), alternating light (hollow bar) and dark (solid bars); ordinate scale for males at right; mean *SEM based on four flight cages, each averaged 2-4 days, 30 June-5 July; two cages were at 37°C and two at 4l”C, but results were same and all four were treated as replicates (MeChrskey, unpub~sh~~.
activity 1990).
among
six species (McCluskey
and Neal,
Control in constant temperature and lighting One might expect then that there is internal control of Right timing. Further evidence is that
rhythmicity remains even when the temperature is held constant. Winged ants from field nest entrances were placed in “flight cages” of ventilated, clear plastic boxes (0.15 x 0.3 x 0.1 m high), each connected to a small dark, moist container. At all hours, light or dark, the constant temperature was like that at flight time in the field; yet the ants flew only in the morning (Fig. I and McCluskey, 1969). This would include the late morning flight time of the field; but there the duration is much shorter, perhaps because the temperature rapidly rises from too cool to too warm. The activity times of maies of two other species (different subfamilies), likewise in constant temperature, are seen in Fig. 2A. Though observed on the same days, note the opposite phases of rhythm. The “dawn” time of harvester ant activity corresponds with the field pre-sunlight flight time; the Argentine ant is not known to have mating flights, though males come to lights at night. The rhythms, including the opposite phase relationship, persist in constant darkness as well as temperature (Fig. 2B). This is an additional, important type of evidence for internal circadian control. The species-specific phase (the “window” suggested by field evidence above), could be set by the
I I I
40-
I I
VC~fY&nn~Mr
Jr3
, I 1 , I
20lo-
o-
~
, I t ,
Fig. 2. Rhythm of male activities in constant temperature and (8) darkness as well. iridomyrmex humilis (Argentine ant, top), number outside plaster nest units; Messor ( = Veromessor) andrei (a dark harvester ant, bottom), counts past point in tube. (A) Alternathtg light and dark. (B) Constant dark (dim red light). Modified from McCluskey, 1958, Fig. 1, and 1963, Fig. 6 (which actually continues very same experiment and ants).
Periodicity and diversity in ant mating flights
start of dawn, as if timed by an internal clock; so many flew at once that they could be heard as a “roar”, though it was of course too dark to see them (Moser, 1967). (2) The hour that winged female harvester ants ran around the surface of a terrarium nest (Fig. 3) was surprisingly consistent from day to day,-the more so because it was in variable office lighting and temperature.
8 7 62
5-
8
4 3
3 tt
: 0 Ii:,! -1 0
12
6
18
24
HOUR
Fig. 3. Rhythm of female presence above ground. Winged female Pogonomyrmex badius, terrarium tank nest (0.3 x 0.3 x 0.8 m) in E. 0. Wilson’s office at Harvard University; a thriving colony, often with 200 workers and several giant majors out at once; variable lighting and temperature from both indoors and nearby open or shut window; mean + SEM based on the five replicate days (28 Feb.6 April, 1960) when females came out and counts were made [McCluskey, unpublished; field mating activities are likewise in the morning (Van Pelt, 1953)].
Acknowledgements-I
thank Hal Reed for his many suggestions, which so improved the manuscript; Paul Kannowski and the late Mary Talbot for permission to use several observations which fill in their published data; and Ed Wilson for the use of his office ant colony. The research presented in Fig. 1 and 3 was supported by NIH Grant GM 11864 and NSF postdoctoral fellowship 49101, respectively.
REFERENCES Holldobler B. (1976) The behavioral ecology of mating in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex).
light-dark cycle, with placement in the window determined by field temperature (or other variable). Loss of female
rhythmicity
After mating, the females of both M. pergandei and P. californicus cease rhythmic behavior, whether of coming out to the arena of an artificial nest, or of electronic- or visually-detected movement within (McCluskey, 1967; McCluskey and Carter, 1969). Such activities appear random, in strong contrast to that before mating flight. The loss is related to mating, because there is no loss after flight itself in flight cages, or after simple wing removal, either artificial or natural by the ants (which usually follows mating). But the loss is dramatic the first day after mating, whether that occurs naturally in the field, or when confined with males in flight cages (but then only if mating can be demonstrated by the presence of sperm in the spermatheca). Such an abrupt loss after mating suggests a special function of the rhythm before mating, perhaps one or more of the following (McCluskey, 1963): internal timing could prepare the ants physiologically for the mating flight; further, their presence at the nest exit at the appropriate flight hour could enable them to perceive environmental time cues such as light or temperature. Phase synchrony within species should facilitate cross-breeding between colonies. Phase difference between species might favor reproductive isolation. CONCLUSION
The diversity and elegant precision of timing outlined above are illustrated in another way by two final examples: (1) Most daily flights of the leafcutting ant Atta “were between 355 and 4a.m.“~before the
texana
243
Behav. Ecol. Sociobiol. 1, 405423.
Hijlldobler B. and Wilson E. 0. (1990) The Ants, Chap. 3. Harvard University Press, Cambridge, MA. Kannowski P. B. (1963) The flight activities of formicine ants. Symp. Genet. Biol. Ital. 12, 74102. Kusnezov N. (1962) El vuelo nuptial de las hormigas. Acta 2001. Lill. 18, 38542.
MacKay E. E. and MacKay W. P. (1984) Apoyo a la actual division generica de hormigas usando etologia comparativo (Hymenoptera, Formicidae). Folia Entomol. Mex. 61, 179-188.
McCluskey E. S. (1958) Daily rhythms in male harvester and Argentine ants. Science 128, 536-537. McCluskey E. S. (1963) Rhythms and clocks in harvester and Argentine ants. Physiol. Zool. 36, 273-292. McCluskey E. S. (1967) Circadian rhythms in female ants, and loss after mating flight. Camp. Biochem. Physiol. 23, 665-677.
McCluskey E. S. (1969) Field and laboratory timing of the flights of a harvester ant. Am. Zool. 9,566 (abstract only). McCluskey E. S. (1973) Generic diversity in phase of rhythm in formicine ants. Psyche 80, 295-304. McCluskey E. S. (1974) Generic diversity in phase of rhythm in myrmicine ants. J. N. Y. Entomol. Sot. 82, 93-102. McCluskey E. S. (1982) Multivariate generic comparison of ant flights. In The Biology of Social Znsecrs (Edited by Breed M. D., Michener C. D. and Evans H. E.), p. 408 (abstract only). Westview Press, Boulder, CO. McCluskey E. S. and Carter C. E. (1969) Loss of rhythmic activity in female ants caused by mating. Comp. Biochem. Physiol. 31, 2 17-226.
McCluskey E. S. and McCluskey D. K. (1984) Hour of mating flight in three species of ants (Hymenoptera: Formicidae). Pan-Pa@ Entomol. 60, 151-154. McCluskey E. S. and Neal J. S. (1990) Hour versus temperature in ant species diversity in field rhythm. Psyche 97, 65-73.
Moser J. C. (1967) Mating activities of Atta texana (Hymenoptera, Formicidae). Insectes Sociaux 14, 295-3 12. Talbot M. (1945) A comparison of flights of four species of ants. Am. Midland Naturalist 34, 504-510. Van Pelt A. (1953) Notes on the above-ground activity and a mating flight of Pogonomyrmex badius (Latr.). J. Tenn. Acad. Sci. 28. 164-168.
PERIODICITY AND DIVERSITY IN ANT MATING FLIGHTS ELW~D
S. MCCLUSKEY
Physiology Department, Loma Linda University, tama Linda, CA 92350, USA. (Received 2 March 1992; accepted 1 April 1992) Abshwt-1.
Plight hours and seasons are alike within species, but differ among species and among
genera. 2. Laboratory studies indicate internal circadian control of the phase relation to the light-dark cycle, with field evidence for modiition by temperature (or other environmental variables). 3. In at least two species there is abrupt loss of obvious rhythm after mating, suggesting some special function before loss, e.g. to facilitate cross-breeding within species or reproductive isolation between
t~RoDu~oN Noteworthy features of the mating system in ants include the special castes involved, the elaborate means for cross-colony synchronization within a species, and the enormous diversity within the family [see Hiilldobler and Wilson (1990) for a comprehensive account]. In many species the winged sexual castes are produced at a certain season. Mating occurs during or following a flight at a characteristic time of day, when males encounter females from other colonies. The inseminated females then start new colonies. This brief review of both published and unpublished studies wilf examine two main questions: how diverse are the flight times among species and genera? and what controls their timing? HOW TAXONOMICALLY DIVERSE ARETHE FLIGHT TIMES? l%e Aights of the colonies of a particular species in a given area are typically at the same time of day
and season (Talbot, 1945; Kannowski, 1963): e.g. Prenalepis imparis, early spring in the warmest part of the day (Talbot, 1945); Solenopsis maniosa, early summer in late afternoon before sunset (McCluskey and McCluskey, 1984). The same phenomenon is illustrated by four species of Pago~arn~rrne~~ all in the same season and locality: colonies of any one species fly at the same hour, but different species at different hours (Hiilldobler, 1976). Not only are flight times more alike within than among species; they are also more alike within than among genera (McCluskey, 1973, 1974, 1982; MacKay and Ma&Lay, 1984). The best illustration of this is from the George Reserve in Michigan, where Paul Kannowski and especially Mary Talbot studied numerous mating flights (at least 34 species, in nine genera), all in one locality. Thus, variability associated with multiple localities is greatly reduced,
increasing the validity of comparison of the ants themselves. When their flight records (largely cited in McCluskey, 1973, 1974) are plotted hour against season (McCluskey, in preparation), the species of each one of the six genera with more than one species are clearly grouped; and on average, each genus overlaps only one of the others. The same pattern is illustrated by flights which were not only all in one locality (Tucuman, Argentina) but also on the same day (Kusnezov, 1962). Of the 15 genera with good flight records, only two had enough species for a good comparison. All four Wenopsis species were flying in the late morning, but no Pfteidole; and all nine PheSole species at the end of the day, but no Sokopsis (compiled from Kusnezov). WHAT CONTROLS THE TYMlNG? Relationship to temperature
Records from the George Reserve were again used, but only those with morning Bights, so as to avoid the complications due to afternoon reversal of temperature. In each one of the six species with enough flights to compare different days (four species of Formica, two of Dolichoderus) the tiights were later the cooler the day (McCluskey, in preparation). But there are limits to such a relationship. For example, if Messar andrei do not fly before the nest is exposed to the sun, they do not fly that day at all (McCluskey, 1963). The same is true for colonies of N. pergandei around Colton, California, if a certain temperature is not reached soon after the nest is exposed to the sun, and of Pogonomyrmex cafifornict~s if they do not fly by noon (McCluskey, unpubtblished). It is as if there were a “time window”, within which flight is affected by temperature or other factors. Consistent with this conclusion is the finding that both hour and temperature seem necessary to explain the diversity of timing of field worker ant
ELWOODS. MCCLUSKEY
242
0
0
12
6
18
24
houw
Fig. I. Rhythmof male and female fIight in constant temperature. Winged Fogonomyrmex californicus (a red harvester ant), alternating light (hollow bar) and dark (solid bars); ordinate scale for males at right; mean *SEM based on four flight cages, each averaged 2-4 days, 30 June-5 July; two cages were at 37°C and two at 4l”C, but results were same and all four were treated as replicates (MeChrskey, unpub~sh~~.
activity 1990).
among
six species (McCluskey
and Neal,
Control in constant temperature and lighting One might expect then that there is internal control of Right timing. Further evidence is that
rhythmicity remains even when the temperature is held constant. Winged ants from field nest entrances were placed in “flight cages” of ventilated, clear plastic boxes (0.15 x 0.3 x 0.1 m high), each connected to a small dark, moist container. At all hours, light or dark, the constant temperature was like that at flight time in the field; yet the ants flew only in the morning (Fig. I and McCluskey, 1969). This would include the late morning flight time of the field; but there the duration is much shorter, perhaps because the temperature rapidly rises from too cool to too warm. The activity times of maies of two other species (different subfamilies), likewise in constant temperature, are seen in Fig. 2A. Though observed on the same days, note the opposite phases of rhythm. The “dawn” time of harvester ant activity corresponds with the field pre-sunlight flight time; the Argentine ant is not known to have mating flights, though males come to lights at night. The rhythms, including the opposite phase relationship, persist in constant darkness as well as temperature (Fig. 2B). This is an additional, important type of evidence for internal circadian control. The species-specific phase (the “window” suggested by field evidence above), could be set by the
I I I
40-
I I
VC~fY&nn~Mr
Jr3
, I 1 , I
20lo-
o-
~
, I t ,
Fig. 2. Rhythm of male activities in constant temperature and (8) darkness as well. iridomyrmex humilis (Argentine ant, top), number outside plaster nest units; Messor ( = Veromessor) andrei (a dark harvester ant, bottom), counts past point in tube. (A) Alternathtg light and dark. (B) Constant dark (dim red light). Modified from McCluskey, 1958, Fig. 1, and 1963, Fig. 6 (which actually continues very same experiment and ants).
Periodicity and diversity in ant mating flights
start of dawn, as if timed by an internal clock; so many flew at once that they could be heard as a “roar”, though it was of course too dark to see them (Moser, 1967). (2) The hour that winged female harvester ants ran around the surface of a terrarium nest (Fig. 3) was surprisingly consistent from day to day,-the more so because it was in variable office lighting and temperature.
8 7 62
5-
8
4 3
3 tt
: 0 Ii:,! -1 0
12
6
18
24
HOUR
Fig. 3. Rhythm of female presence above ground. Winged female Pogonomyrmex badius, terrarium tank nest (0.3 x 0.3 x 0.8 m) in E. 0. Wilson’s office at Harvard University; a thriving colony, often with 200 workers and several giant majors out at once; variable lighting and temperature from both indoors and nearby open or shut window; mean + SEM based on the five replicate days (28 Feb.6 April, 1960) when females came out and counts were made [McCluskey, unpublished; field mating activities are likewise in the morning (Van Pelt, 1953)].
Acknowledgements-I
thank Hal Reed for his many suggestions, which so improved the manuscript; Paul Kannowski and the late Mary Talbot for permission to use several observations which fill in their published data; and Ed Wilson for the use of his office ant colony. The research presented in Fig. 1 and 3 was supported by NIH Grant GM 11864 and NSF postdoctoral fellowship 49101, respectively.
REFERENCES Holldobler B. (1976) The behavioral ecology of mating in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex).
light-dark cycle, with placement in the window determined by field temperature (or other variable). Loss of female
rhythmicity
After mating, the females of both M. pergandei and P. californicus cease rhythmic behavior, whether of coming out to the arena of an artificial nest, or of electronic- or visually-detected movement within (McCluskey, 1967; McCluskey and Carter, 1969). Such activities appear random, in strong contrast to that before mating flight. The loss is related to mating, because there is no loss after flight itself in flight cages, or after simple wing removal, either artificial or natural by the ants (which usually follows mating). But the loss is dramatic the first day after mating, whether that occurs naturally in the field, or when confined with males in flight cages (but then only if mating can be demonstrated by the presence of sperm in the spermatheca). Such an abrupt loss after mating suggests a special function of the rhythm before mating, perhaps one or more of the following (McCluskey, 1963): internal timing could prepare the ants physiologically for the mating flight; further, their presence at the nest exit at the appropriate flight hour could enable them to perceive environmental time cues such as light or temperature. Phase synchrony within species should facilitate cross-breeding between colonies. Phase difference between species might favor reproductive isolation. CONCLUSION
The diversity and elegant precision of timing outlined above are illustrated in another way by two final examples: (1) Most daily flights of the leafcutting ant Atta “were between 355 and 4a.m.“~before the
texana
243
Behav. Ecol. Sociobiol. 1, 405423.
Hijlldobler B. and Wilson E. 0. (1990) The Ants, Chap. 3. Harvard University Press, Cambridge, MA. Kannowski P. B. (1963) The flight activities of formicine ants. Symp. Genet. Biol. Ital. 12, 74102. Kusnezov N. (1962) El vuelo nuptial de las hormigas. Acta 2001. Lill. 18, 38542.
MacKay E. E. and MacKay W. P. (1984) Apoyo a la actual division generica de hormigas usando etologia comparativo (Hymenoptera, Formicidae). Folia Entomol. Mex. 61, 179-188.
McCluskey E. S. (1958) Daily rhythms in male harvester and Argentine ants. Science 128, 536-537. McCluskey E. S. (1963) Rhythms and clocks in harvester and Argentine ants. Physiol. Zool. 36, 273-292. McCluskey E. S. (1967) Circadian rhythms in female ants, and loss after mating flight. Camp. Biochem. Physiol. 23, 665-677.
McCluskey E. S. (1969) Field and laboratory timing of the flights of a harvester ant. Am. Zool. 9,566 (abstract only). McCluskey E. S. (1973) Generic diversity in phase of rhythm in formicine ants. Psyche 80, 295-304. McCluskey E. S. (1974) Generic diversity in phase of rhythm in myrmicine ants. J. N. Y. Entomol. Sot. 82, 93-102. McCluskey E. S. (1982) Multivariate generic comparison of ant flights. In The Biology of Social Znsecrs (Edited by Breed M. D., Michener C. D. and Evans H. E.), p. 408 (abstract only). Westview Press, Boulder, CO. McCluskey E. S. and Carter C. E. (1969) Loss of rhythmic activity in female ants caused by mating. Comp. Biochem. Physiol. 31, 2 17-226.
McCluskey E. S. and McCluskey D. K. (1984) Hour of mating flight in three species of ants (Hymenoptera: Formicidae). Pan-Pa@ Entomol. 60, 151-154. McCluskey E. S. and Neal J. S. (1990) Hour versus temperature in ant species diversity in field rhythm. Psyche 97, 65-73.
Moser J. C. (1967) Mating activities of Atta texana (Hymenoptera, Formicidae). Insectes Sociaux 14, 295-3 12. Talbot M. (1945) A comparison of flights of four species of ants. Am. Midland Naturalist 34, 504-510. Van Pelt A. (1953) Notes on the above-ground activity and a mating flight of Pogonomyrmex badius (Latr.). J. Tenn. Acad. Sci. 28. 164-168.
