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Critical thermal maxima and body size positively correlate in red imported fire ants, Solenopsis invicta.

Temperature variations associated with changing climates are strongly affecting the geographical distribution, foraging activity, and diversity of ectotherms across the globe (Pelini et al., 2011). In particular, small changes in temperature may represent a big challenge for ectotherms with low heat tolerance or those that already survive close to their upper thermal tolerance limit (Baudier et al., 2015). Among terrestrial invertebrates, ants represent an ideal group to investigate the link between thermal ecology and climate warming (Del Toro et al., 2015), as they are relatively easy to collect, house, and identify. To date, limited work has been conducted on ant thermal tolerance and body size. Most studies that account for both ant critical thermal maxima and body size have been confined to the genus Cataglyphis and show mixed results. Some authors (Cerda and Retana, 2000; Clemencet et al., 2010) report that colonies of Cataglyphis cursor differ in their critical thermal maximum (CTmax) by size; larger (foraging) workers have a higher thermal tolerance and smaller (nest) workers show lower heat tolerance. Two other species of Cataglyphis show different relationships between body size and thermal tolerance (Cerda and Retana, 2000). Cataglyphis velox workers are highly polymorphic (Cerda and Retana, 1997) and exhibit a strong relationship between body size and foraging activity as well as a positive relationship between body size and thermal tolerance; larger workers forage during the hot hours of the day while smaller workers forage under low temperature conditions (Cerda and Retana, 2000). However, C. rosenhaueri is characterized by small ants that forage independently of the environmental temperature and body size (Cerda and Retana, 2000).

While the relationship between body size and critical thermal maxima is confounded by foraging behavior in Cataglyphis ants, other more-general patterns have also been observed, and it has been demonstrated that body size directly influences physiology in numerous species (Peters, 1986). Larger ants have a slower desiccation rate than do smaller ants due to a smaller surface-area-to-volume ratio (Hood and Tschinkel, 1990; Cerda and Retana, 2000). Kaspari et al. (2014) found a positive relationship between body size and critical thermal maxima among species of tropical ants; however, Verble-Pearson et al. (2015) found a strong inverse correlation between ant body size and CTmax among species of temperate ants.

Red imported fire ants (Solenopsis invicta) are polymorphic (Tschinkel, 1988) and exhibit allometric castes (Tschinkel, 2003); therefore, they are an ideal species in which to study the influence of body size on intraspecific thermal maxima. Additionally, fire ants are conspicuous, easily collected, and have been extensively studied due to their invasion of the southeastern United States. Fire ant desiccation resistance is reported by Phillips et al. (1996), metabolic rates are reported by Vogt and Appel (1999), and thermal limits are reported by Cokendolpher and Phillips (1990). However, none of these studies address ant body size and its potential impact on these physiological metrics. In this study, we examined fire ant critical thermal maxima and its relationship to body size. We hypothesized that there is a relationship between thermal physiology and body size in S. invicta and that critical thermal maxima would increase with increasing ant body size.

To test the relationship between body size and thermal tolerance in S. invicta, we collected workers from 35 colonies (with a longitude-latitude minute of 100 m distance between colonies) from areas within and surrounding Lubbock, Texas (33[degrees]34'N, 101[degrees]53'W) from April-June 2014. Collected workers were housed in plastic containers at 22[degrees]C with ad libitum water and honey for 12-72 h. Acclimation periods were broad as a result of many colonies being collected at once, which resulted in delays in processing (Lutterschmidt and Hutchinson, 1997; Lighton and Turner, 2004). We divided workers (major, media, minor) from each colony according to their body size (n = 20 individuals per size). Workers were sorted based on a visual assessment of their size relative to other members of the colony but were later measured to confirm visual assessments. Ants of each subset were placed in 3 x 7-cm cylindrical thin plastic vials in a water bath with an initial temperature of 28[degrees]C (the temperature of tap water used to fill the water bath). Each vial contained two individuals of a given size, and a single water bath trial contained no more than 10 vials (or 20 individuals). We progressively raised the temperature of the hot-water bath (1[degrees]C/min) from 28[degrees]C past the CTmax of all individuals (as per Verble-Pearson et al., 2015) and observed ant behaviors from a fixed position above the water. CTmax was defined as the point at which ants lost coordination and the ability to right themselves (loss of righting response; Huey et al., 1992) or a state of partial paralysis (Cerda et al., 1998), whichever occurred first. The temperature at which one of these behaviors occurred was recorded for all individuals and regressed against their body size. Finally, as a negative control against factors such as suffocation, a colony was kept in the water bath at 28[degrees]C inside glass vials for 3 h and survival was recorded. Digitally displayed water bath temperatures were calibrated in advance of data collection using a glass thermometer. Vial internal temperatures were verified using HOBO[TM] data loggers, models U12-006 and TMC6-HE, accurate to 0.25[degrees]C (Onset Computer Corporation, Bourne, Massachusetts).

[FIGURE 1 OMITTED]

We measured ant mass using 100 individuals of each subset and calculated the average mass for each of the three subsets. In addition, we used standard morphometrics (tibial length, total body length, head width including the eyes; Holldobler and Wilson, 1990) to measure euthanized workers under a dissecting microscope. Of these, tibial length correlated best with ant mass, and we regressed it against CTmax (Fig. 1).

Data were analyzed using a one-way analysis of variance (ANOVA) and Tukey multiple comparisons tests in JMP statistical software (SAS Institute, Cary, New York), and plots were constructed in SigmaPlot[TM] Version 12.0 (Systat Software, San Jose, California).

Workers of all colonies responded to increasing temperature with a characteristic set of behaviors. After a few minutes of acclimation to the vials, ants started exploring and then transitioned from exploring to frenetic digging. Larger workers began frenetic digging earlier compared to smaller ones. Immediately before reaching their CTmax, workers calmed, became immobile, or both. CTmax was determined for large, medium, and small workers (n > 5/colony per size) of S. invicta (Table 1). Minor workers had [greater than or equal to] 0.5[degrees]C lower thermal maxima than did either the media or major workers, which did not differ from one another (df = 34, F = 11.53, P < 0.0001, Fig. 2). Tibial length as a surrogate for mass and CTmax were also significantly correlated ([R.sup.2] = 0.19, P < 0.0001; Fig. 2).

These results are congruent with results from Cerda and Retana (1997) on Cataglyphis desert ants, where smaller workers showed a lower thermal tolerance than did larger workers. Larger workers with higher thermal tolerances represent an advantage for the colony. Larger workers showed a higher resistance to heat and higher desiccation resistance than did the smaller nest mates, possibly due to their lower surface-area-to-volume ratios (Hood and Tschinkel, 1990; Phillips et al., 1996; Cerda and Retana, 2000; Clemencet et al., 2010). For the colony, larger workers with a lower desiccation rate, lower maintenance costs, and a higher CTmax provided advantages in terms of the services those workers are capable of providing and the conditions under which they were able to function (Wilson, 1976; Beshers and Traniello, 1994; Clemencet et al., 2008; Clemencet et al., 2010; Shik 2010).

It remains unclear why there was no difference in the thermal maxima of medium and large ants, despite a large difference in body size. Large and medium workers may face similar thermal challenges due to similar tasks or roles in the colony; however, this remains to be empirically tested. In particular, an investigation of the association between thermal tolerance, body size, and microhabitat use in fire ant colonies is needed. Recent studies (Baudier et al., 2015) highlight the relationship between CTmax and microhabitat use; above-ground ant species showed a higher heat tolerance than the below-ground species. The utilization of similar microhabitats (and thus, the experience of similar microclimates) by medium and large fire ant workers may explain the lack of difference in CTmax between the two groups. During the hottest hours of the day, medium and large workers may be responsible for similar above-ground activities whereas the activity of small fire ants may be primarily below ground; however, this remains to be empirically tested.

Major workers with a higher CTmax are especially important for the colony, as their foraging activity can occur during hotter periods (Cerda and Retana, 2000), particularly during the warm season of the year when the colony is most active. Most of the foraging activity in fire ants develops in underground tunnels, but having larger workers in a colony may be useful for occasional aboveground foraging bouts. Further, soil temperatures increase during prolonged periods of high ambient temperatures, so foraging activity of larger workers may represent the only way to provide food for the colony during these times; however, this remains to be tested.

Energetically, larger workers can represent either a cost for the colony, as they are more expensive to produce and maintain (Holldobler and Wilson, 1990), or a benefit (Shik, 2010) as studies show that major workers require 30% fewer calories per month per milligram than do smaller ants (Calabi and Porter, 1989). On an individual basis, the production of larger workers is up to four times more expensive than that of smaller nest mates (Calabi and Porter, 1989). However, the total biomass of a mature fire ant colony (4-6 y old) is 70% made up of larger workers (Tschinkel, 1988), suggesting that having these workers or, in general, caste diversity benefits the colony (Retana and Cerda, 1994; Fjerdinsgtad and Crozier, 2006; Gravish et al., 2012), despite their high production and maintenance costs (Calabi and Porter, 1989; Holldobler and Wilson, 1990).

Finally, polymorphic workers of varying thermal tolerances may benefit the invasiveness of red imported fire ants as compared to monomorphic ant species (Trager, 1991). The thermal adaptive capacity of this species may facilitate colonization of new areas and environments and, as climates warm, this species has the potential to maintain its geographical range and further increase its distribution in North America (Bellard et al., 2013) into regions that were unoccupied in the past (Thuiller et al., 2007). The consequences of these range expansions are likely to have economic and agricultural impacts (Trager, 1991).

Future thermal ecology studies of S. invicta should focus on three factors: shifts in global climate, plasticity of thermal tolerance, and dispersal ability. Finally, we did not test colony age as a factor influencing CTmax, but future studies should also consider this. Bowler and Terblanche (2008) underlined the importance of age and ontogeny in insect thermal tolerance; these factors can increase or decrease the heat tolerance of an organism. In conclusion, this research represents a starting point for future works on thermal physiology and its relationship to the morphology of S. invicta.

[FIGURE 2 OMITTED]

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Submitted 25 February 2015.

Acceptance recommended by Associate Editor, Jerry Cook, 3 January 2016.

Clara Frasconi Wendt, Robin Verble-Pearson *

Department of Natural Resource Management, Texas Tech University, Lubbock, TX 79409

* Correspondent: robin.verble@ttu.edu
Table 1--Measurements of mass (g; average mass of 100
individuals per group) and critical thermal maximum (CTmax;
[degrees]C) among the three body sizes of Solenopsis invicta (large,
medium and small) from areas within and around Lubbock,
Texas, collected April-June 2014. N = total number of colonies
used to calculate CTmax.

Body size   Mean mass (g)   CTmax ([degrees]C)   SE      N

Large       0.003142        46.46                0.084   35
Medium      0.001279        46.39                0.084   35
Small       0.000466        45.93                0.084   35
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Author:Wendt, Clara Frasconi; Verble-Pearson, Robin
Publication:Southwestern Naturalist
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Date:Mar 1, 2016
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