Western North American Naturalist

Volume 63 Number 1 Article 17

1-31-2003

Effect of temperature on brood relocation in salinus (Hymenopteria: Formicidae)

Kirk E. Anderson Boise State University, Boise, Idaho

James C. Munger Boise State University, Boise, Idaho

Follow this and additional works at: https://scholarsarchive.byu.edu/wnan

Recommended Citation Anderson, Kirk E. and Munger, James C. (2003) "Effect of temperature on brood relocation in Pogonomyrmex salinus (Hymenopteria: Formicidae)," Western North American Naturalist: Vol. 63 : No. 1 , Article 17. Available at: https://scholarsarchive.byu.edu/wnan/vol63/iss1/17

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Western North American Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. Western North American Naturalist 63(1), ©2003, pp. 122–128

EFFECT OF TEMPERATURE ON BROOD RELOCATION IN POGONOMYRMEX SALINUS (: FORMICIDAE)

Kirk E. Anderson1,2 and James C. Munger1

ABSTRACT.—Brood movement in response to temperature by Pogonomyrmex salinus (seed-harvester ) nurse workers was examined in the sagebrush steppe of southeast Idaho. Shading the mound surface of P. salinus colonies at dawn caused a decrease in mound temperature and led to significantly less brood accumulation near the surface. In a related experiment, a lab colony of P. salinus was offered an artificial thermal gradient during the cool/dark portion of the daily cycle. Nurse workers removed brood from the 21°–22°C range to soils with temperatures between 29°C and 36°C. Daily brood relocation by P. salinus nurse workers is a highly flexible behavior, capable of immediate response to temperature, and does not appear to follow a strict endogenous rhythm.

Key words: thermoregulation, endogenous, rhythm, circadian, Pogonomyrmex salinus, harvester ant, Hymenoptera, Great Basin.

Nearly all organisms show predictable daily follows a strict endogenous rhythm where nurse cycles of activity. Although some cycles are a workers relocate brood at 2 critical times of response to environmental cues, most are con- the day, when environmental temperature is trolled by an internal biological clock known expected to reach its maximum and minimum as an endogenous circadian (daily) rhythm. An values (Roces 1995). Nurse workers of Pogono- endogenous rhythm persists in the absence of myrmex salinus and P. occidentalis also trans- environmental time cues and will “free-run,” port brood throughout the nest chambers, but thereby revealing its own natural period (Saun- this behavior seems highly dependent on hourly ders 1976). An endogenous rhythm allows an temperature cues (Anderson and Munger per- organism to anticipate and exploit predictable sonal observation). Extensive chamber area is environmental variation, whereas a direct re- present near the nest surface of many har- sponse to environmental cues allows an organ- vester ant species (Cole 1994, Tschinkel 1999) ism to escape from or exploit unpredictable and may have functional value in brood thermo- environmental variation. Some possess regulation. strict endogenous rhythms (Alpatov et al. 1999); The northernmost species of Pogonomyr- others are largely dependent on environmen- mex are P. salinus and P. occidentalis. These tal cues (Odhiambo 1966). Most investigations species are ecologically similar; both inhabit thus far have shown a mixture of strong en- temperate climates, exhibit a daily cycle of dogenous components modified by exogenous brood relocation during the warm season, and components (Saunders 1976, McCluskey and construct a nest surmounted by a conical Soong 1979, Roces and Nunez 1996). mound. Cole (1994) considered the nest-cone In ant colonies internal nest temperatures of P. occidentalis to be a morning solar collec- directly influence nurse worker activity and tor. Brood individuals are taken into the nest- the rate of brood development (MacKay 1985, cone in the morning as the nest-cone warms, Porter and Tschinkel 1993). Bushinger (1973) and then moved to lower portions of the nest reported that 5 temperate species not only tol- as the nest-cone attains overly high tempera- erate daily nest temperature variations, but tures. At dusk, brood individuals remain in require them for larval development. Temper- lower portions of the nest while workers ature selection for brood depends on the be- return to the chambers in the nest-cone and havior of nurse workers (Roces and Nunez presumably remain there until dawn, perhaps 1989). The temperate species Camponotus mus in anticipation of warming. Cole (1994) noted

1Department of Biology, Boise State University, 1910 University Drive, Boise, ID 83725. 2Present address: Department of Biology, Arizona State University Main, Tempe, AZ 85287-1501.

122 2003] RESPONSE OF POGONOMYRMEX SALINUS TO TEMPERATURE 123 that those workers in the nest-cone chambers to a depth of 20 cm, alternating between shaded before dawn are concentrated on the eastern and nonshaded colonies. The excavation pro- side of the nest-cone, although that portion of cedure was as follows: a shallow groove was the nest-cone is not any warmer at that time of etched east to west across the surface of each day. This apparent anticipatory behavior in P. nest-cone to divide the colony into halves. occidentalis suggests the presence of an en- Then, one-half of the nest-cone was removed dogenous rhythm, but also could be explained in layers to expose brood chambers, while the by exogenous factors. other half of the nest-cone was used to mea- Is the brood-tending behavior of P. salinus sure chamber depth, with the first detected capable of exogenous control, showing imme- chamber representing 0 cm. The number and diate response to temperature, or is it under depth of brood individuals and the tempera- strict endogenous control, entrained by daily ture of chambers containing brood were re- cycles of light and/or temperature? In the pre- corded. The total number of brood individuals sent study we disrupted the typical daily cycle above 20 cm in shaded vs. nonshaded colonies of environmental cues to determine the extent was analyzed using an independent-samples t of endogenous control. Because brood-tending test. For graphing purposes brood were classi- behavior is normally performed in the dark, fied as (<5) per chamber, (5–10) per chamber, we manipulated the environmental cue of (10–20) per chamber, and (>20) per chamber. temperature. Specifically, we examined how Temperature was recorded from the surface brood relocation in P. salinus is affected by a substrate of each nest-cone prior to excavation shade-induced disruption of the natural morn- and at depths of 2.5 cm, 5 cm, and 10 cm. Soil ing warming of nest-cones in the field, and a temperature was measured using a 40-gauge heat-induced disruption of the normally cool/ Cu-CuNi thermocouple (response time <5 dark period in a laboratory nest. seconds) read by an Omega HH25TC digital thermocouple reader. MATERIALS AND METHODS Lab Study Field Study A colony consisting of a queen, approximate- This study was performed on 23 July 1996 ly 250 workers, and 80 brood (mostly pupae in an area of mixed sagebrush (Artemisia tri- and final instars) was excavated from the field dentata) and cheatgrass (Bromus tectorum) site. The colony, including nest soil, was placed south of Kuna, Idaho. The terrain is predomi- in a vertical glass enclosure that measured 50 nantly flat, and soils are of moderately deep × 65 × 1 cm, and topped horizontally with a 20 gravelly loam. Twenty-five Pogonomyrmex sal- × 30 × 8-cm foraging area. The soil within the inus colonies along a roadside were selected enclosure was equipped with 7 Cu-CuNi ther- for study. All colonies had the same slope and mocouple wires at depths of 2.5, 5, 10, 20, 30, aspect and were surmounted by a well-formed 40, and 50 cm. The lower 40 cm of the vertical nest-cone. All colonies were mature, active, and glass enclosure was covered from the outside received about the same daily solar exposure. with a 1-foot-thick soil/sand mixture packed Just before sunrise, 13 of the nest-cones firmly against the outside. This soil layer was were shielded from the sun with stiff card- moistened and shaded with cardboard to sim- board (approximately 1 m square) supported ulate the stability of natural ground tempera- at a 45° angle by 3 wooden stakes. The 12 con- ture. The foraging area was filled with a 2-cm- trol colonies were disturbed in the same man- deep layer of soil and exposed to the solar ner but not shaded. Nonshaded colonies alter- cycle to maintain natural light and tempera- nated spatially with shaded colonies. Shade ture fluctuations and any endogenous rhythm construction began at 0615 hours and was present in P. s a linus. The colony was allowed completed by 0730; sunrise was at 0633 hours. to reestablish its nest structure with the forag- A mature harvester ant nest may extend ing area and upper 10 cm of the glass enclo- several feet below the surface, but only the sure exposed to natural outdoor conditions: uppermost portions of the nests are affected LD 16:8 cycle and naturally occurring July/ by daily temperature cycles. Between 0829 August climate. Stored seed caches from the and 1130 hours, all 25 colonies were excavated natural nest were transferred to the laboratory 124 WESTERN NORTH AMERICAN NATURALIST [Volume 63 nest, and the colony was given additional seed hour, while surface temperatures of nonshaded (Lepidium perfoliatum) to harvest from the colonies ranged from 22.8°C to 48.8°C, and foraging area. increased at a rate of 7°C per hour. After 3 days the colony had established an extensive network of chambers and tunnels in Lab Study the soil. The nest had a 2-dimensional mor- Location of brood in the artificial nest phology resembling a 1-cm slice of naturally shifted markedly in response to the thermal occurring nests, and the colony had resumed gradient (Fig. 2). Temperatures in the 35–50 normal daily foraging cycles. The brood was cm region of the nest were relatively unaf- tended by about 50 nurse workers and was fected by the addition of the thermal gradient: concentrated near the queen in 1 medium and 20.5°–21.3°C before heat was applied and 3 large chambers at depths of 35, 40, 45, and 20.9°–22.5°C during the experiment. Two hours 47 cm. after the gradient became stable, only 20% of On the 4th day, the colony was offered an brood remained in the region (35–50 cm) where artificial thermal gradient during the middle all brood had been located prior to presenta- of the dark cycle. A 30-cm-square heating pad tion of the gradient. was attached to one side of the glass at the top At 2400 hours very few brood individuals of the nest. We created a thermal gradient by had changed position relative to temperature, placing cardboard of varying thickness between and approximately 40% of brood were being the heating pad and the glass of the nest. Tem- carried by nurse workers. No net pattern of peratures in this gradient ranged from 39°C at brood movement was evident. By 0130, approx- 2.5 cm to 21°C at 50 cm. Brood individuals imately 25% of brood were stationary in warmer were initially concentrated 5–17 cm below the locations, nurse workers were carrying 65% of heat source. Heat was applied at 2330 hours, brood, and the entire colony was very active. and a stable thermal gradient was achieved By 0230, most brood individuals were concen- within 30 minutes. Brood location and related trated at a depth of 20–30 cm in 4 large cham- observations were recorded every 30 minutes bers with temperatures in the 29.2°–36.4°C between 2330 and 0400. range (Fig. 2). Also at 0230, worker movement in the 39.5°C chambers at a depth of 10 cm RESULTS was most transient, and brood individuals were not deposited there but were quickly Field Study transported through that region of the gradient. No brood individuals were present above The artificial temperature gradient unex- 20 cm in either shaded or nonshaded colonies pectedly and differentially dried the soil with- excavated between 0830 and 0900 hours. in the artificial nest, creating drier soil patches From 0900 to 1130, shaded colonies contained within the walls of the warmest chambers. At significantly less brood in chambers above 20 0300 hours lines were drawn on the glass to cm than nonshaded colonies, t (15) = 6.93; P delineate dry from moist soil. By 0330, the < 0.0001. Sample means were 6.3 for shaded moist soil had been reduced from 45% to 35% colonies and 104.3 for nonshaded colonies. of the total chamber area. All but a few stray From 0900 to 1130 hours, brood were present brood individuals had been crowded into the at a depth of 0–2.5 cm in all nonshaded moist patches of the 29.2°–36.4°C chambers. colonies, while brood were present at this same depth in the shaded colonies on only 2 DISCUSSION occasions, and in far fewer numbers (Fig. 1). One of these occasions represents the highest Our results strongly indicate that brood surface temperature attained by a shaded relocation in P. salinus is highly sensitive to colony (29.8°C at 1058 hours). hourly temperature changes and is not a strict Shading reduced the surface temperature circadian rhythm. First, if a strict daily rhythm of the nest-cone and brood chambers 2.5 cm controlled brood relocation in P. s a linus, brood deep, but differences were not as great at in shaded colonies would be expected to depths of 5 and 10 cm. Surface temperatures occupy chambers close to the surface about of shaded colonies ranged from 20.9°C to the same time as brood in nonshaded colonies. 29.8°C, and increased at a rate of 2.5°C per However, we found that brood movement in 2003] RESPONSE OF POGONOMYRMEX SALINUS TO TEMPERATURE 125

Fig. 1. Brood abundance and depth in 12 nonshaded (A) and 13 shaded (B) colonies. Data recorded between 0830 and 1130 hours, 23 July 1996, from 25 separate mounds with the same general substrate, shape, and solar exposure. An X indicates no brood detected in that colony to a depth of 20 cm. 126 WESTERN NORTH AMERICAN NATURALIST [Volume 63

Fig. 2. Brood abundance and depth relative to temperature recorded every half hour from 2330 to 0400 hours follow- ing presentation of a thermal gradient. Heat was applied to the artificial nest between 0 cm and 30 cm (indicated by the dotted line) at 2330. The thermal gradient (temperatures in bold) became stable at 2400 hours and remained stable throughout the experiment. The bold line shows the change in mean brood depth over time.

shaded colonies did not occur at the time of temperature extremes (Roces 1995). The pre- day mounds are usually warmed by the sun, sent study does not exclude the possibility of but instead depended on the temperature of an endogenous brood-relocation rhythm in P. the nest-cone. Second, if nurse workers were salinus. However, it is clear that proximal tem- controlled by a strict endogenous rhythm, no perature cues can modify or override any en- immediate response would be expected to dogenous rhythm controlling brood care in P. artificial heat applied at a time when the soil is salinus. normally cool. However, we found that artifi- The ability to respond directly to proximal cial heat caused significant brood relocation temperature cues would be adaptive for activi- 10 hours prior to the time brood are usually ties that rely on temperature, such as brood translocated in the field. In both experiments relocation (as has been shown in this study) nurse workers of P. salinus were highly re- and foraging. Harvester ant foragers show sig- sponsive to sudden changes in the normal nificant nonrhythmic activity in response to temperature cycle. temperature. McClusky and Neal (1990) con- Our results contrast with those of Roces cluded that diversity between the foraging and Nunez (1996) for another temperate species, patterns of 6 species of desert could be Camponotus mus. We found that P. salinus explained by a circadian rhythm heavily modi- selected high temperatures for brood during fied by temperature response. Morton and the cool/dark phase of the diel cycle. How- Davidson (1988) found that the foraging of 4 of ever, C. mus did not tolerate a 3-hour advance 10 harvester ant species was strictly nocturnal in their natural temperature cycle. Instead, C. or diurnal, apparently under endogenous con- mus nurse workers responded to an advanced trol, while foraging of the other 6 was highly thermal cycle by removing brood from an area responsive to temperature. In the genus Pogono- of unexpected warm temperature to an area myrmex, an endogenous rhythm apparently with cooler temperature. It is apparent that P. aids the timing of foraging in P. californicus salinus have a different mode of thermoregula- and P. rugosus (McCluskey and Soong 1979). tory behavior than that found in C. mus, in Even when a rhythm is evident in harvester which an endogenous daily rhythm triggers a ants, it appears to be easily overridden or at thermal-searching behavior in anticipation of least frame-shifted by unpredictable environ- 2003] RESPONSE OF POGONOMYRMEX SALINUS TO TEMPERATURE 127 mental variation. Pogonomyrmex salinus for- LITERATURE CITED ages during midday when clouds cover the sun or a tree casts a shadow across the mound ALPATOV, A.M., V.A. ZOTOV, W.B. TSHERNYSHEV, AND W. J. RIETVELD. 1999. Endogenous circadian rhythm is surface (Willard and Crowell 1965). During ab- crucial tool for survival of the sand-desert tenebri- normally hot summer conditions, many species onid beetle Trigonoscelis gigas Reitter. Biological of harvester ants will shift from diurnal to Rhythm Research 30:104–109. nocturnal foraging (Cole 1932, Tevis 1958, BUSHINGER, A. 1973. The role of daily temperature rhythms McCluskey 1963, Whitford and Ettershank in brood development of ants of the tribe Leptotho- racini (Hymenoptera: Formicidae). Pages 229–232 in 1975, Smith et al. 1987). These studies suggest W. Weiser, editor, Effects of temperature on ecto- that immediate response to temperature may thermic organisms: ecological implications and mech- be as influential as light or temperature cycles anisms of compensation. Springer Verlag. in coordinating the daily foraging activity of CASSILL, D.L., AND W.R. TSCHINKEL. 2000. Behavioral and developmental homeostasis in the fire ant, Sole- harvester ants. nopsis invicta. Journal of Phisiology 46:933–939. Activity patterns in harvester ants are strong- COLE, A.C. 1932. Notes on the ant Pogonomyrmex califor- ly affected by moisture, and many species of nicus, Buckley (Hymenoptera: Formicidae). Entomo- Pogonomyrmex will forage at odd times if the logical News 113–115. COLE, B.J. 1994. Nest architecture in the western har- soil is wet (Whitford and Ettershank 1975, vester ant, Pogonomyrmex occidentalis (Cresson). Gordon 1991). Brood individuals have a thin Insectes Sociaux 41:401–410. cuticle and are more sensitive than adults to GORDON, D.M. 1991. Behavioral flexibility and the forag- conditions of low moisture. Moisture patterns ing ecology of seed harvesting ants. American Natu- in the nest soils provide an important humid- ralist 138:379–411. MACKAY, W.P. 1981. A comparison of the nest phenologies ity gradient that harvester ants can exploit to of three species of harvester ants (Hymenoptera: protect their brood from desiccation (MacKay Formicidae). Psyche 88:25–74. 1981). The effect of humidity on larval devel- ______. 1985. Temperature modifications of the nest of opment was dramatic in the fire ant Solenopsis Pogonomyrmex montanus (Hymenoptera: Formici- invicta. Larvae in chambers with less than dae). Southwestern Naturalist 30:307–309. MCCLUSKEY, E.S. 1963. Rhythms and clocks in harvester 100% humidity were not fed by workers, died and Argentine ants. Physiological Zoology 36:273–292. of starvation, and were eventually cannibal- MCCLUSKEY, E.S., AND J.S. NEAL. 1990. Hour versus tem- ized (Cassill and Tschinkel 2000). In the lab perature in ant species diversity in field rhythm. portion of the present study, nurse workers Psyche 97:65–74. MCCLUSKEY, E.S., AND S.A. SOONG. 1979. Rhythm variables continually moved brood from dry to moist soil as taxonomic characters in ants. Psyche 86:91–102. within the chambers, suggesting that brood MORTON, S.R., AND D.W. DAVIDSON. 1988. Comparative relocation behavior in P. salinus is influenced structure of harvester ant communities. Ecological directly by humidity. Monographs 58:19–38. ODHIAMBO, T.R. 1966. The metabolic effects of the corpus In conclusion, P. s a linus nurse workers are allatum hormone in the desert locust: spontaneous not strictly tied to an endogenous rhythm, but locomotor activity. Journal of Experimental Biology instead exhibit a high degree of behavioral 45:51–63. flexibility in moving brood to temperatures PORTER, S.D., AND W.R. TSCHINKEL. 1993. Fire ant ther- mal preferences: behavioral control of growth and and possibly humidity levels that facilitate metabolism. Behavioral Ecology and Sociobiology brood development. Further investigations are 32:321–329. required to determine the influence of tem- ROCES, F. 1995. Variable thermal sensitivity as output of a perature cycles and humidity on brood-reloca- circadian clock controlling the bimodal rhythm of tion behavior. This short-term study addressed temperature choice in the ant Camponotus mus. Journal of Comparative Physiology 177:637–643. critical hours of the temperature cycle within ROCES, F., AND J.A. NUNEZ. 1989. Brood translocation and a single day. To determine if an endogenous circadian variation of temperature preference in the rhythm entrained by temperature is present in ant Camponotus mus. Oecologia 81:33–37. P. salinus, the brood relocation behavior of ______. 1996. A circadian rhythm of thermal preference in the ant Camponotus mus: masking and entrainment nurse workers should be recorded for several by temperature cycles. Physiological Entomology 21: consecutive days in a fixed-temperature gradi- 138–142. ent void of usual environmental cues. Future SAUNDERS, D.S. 1976. Insect clocks. Pergamon Press Ltd., studies should explore the interaction of tem- Elmsford, New York. 280 pp. perature and moisture, as nurse workers SMITH, S.D., W.E. SMITH, AND D.T. PATTEN. 1987. Effects of artificially imposed shade on a Sonoran Desert appear to respond simultaneously to unex- ecosystem: and soil chemistry responses. pected changes in these variables. Journal of Arid Environments 13:245–257. 128 WESTERN NORTH AMERICAN NATURALIST [Volume 63

TEVIS, L. 1958. Interrelations between the harvester ant WILLARD, J.R., AND H.H. CROWELL. 1965. Biological activi- Veromessor pergandei (Mayr) and some desert ephe- ties of the harvester ant Pogonomyrmex owyheei in merals. Ecology 39:695–704. central Oregon. Journal of Economic Entomology TSCHINKEL, W.R. 1999. Sociometry and sociogenesis of 58:484–489. colonies of the harvester ant, Pogonomyrmex badius: distribution of workers, brood and seeds within the Received 20 December 2000 nest in relation to colony size and season. Ecological Accepted 17 January 2002 Entomology 24:222–237. WHITFORD, W.G., AND G. ETTERSHANK. 1975. Factors affecting foraging activity in Chihuahuan Desert har- vester ants. Environmental Entomology 4:689–696.