Behavioral Ecology Vol. 15 No. 3: 390-395
Behavioral Ecology vol. 15 no. 3 © International Society for Behavioral Ecology 2004; all rights reserved
Reproductive decision-making in the termite, Cryptotermes secundus (Kalotermitidae), under variable food conditions
a Universität Regensburg, Biologie I, 93040 Regensburg, Germany, and b CSIRO-Entomology, GPO 1700, Canberra ACT 2601, Australia
Address correspondence to J. Korb. E-mail: judith.korb{at}biologie.uni-regensburg.de.
Received 26 October 2002; revised 20 May 2003; accepted 24 June 2003.
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ABSTRACT |
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Relatedness concepts have dominated the discussion on the evolution and maintenance of eusociality in social insects. In the diploid termites, explanations based on relatedness asymmetries have been less relevant than in the Hymenoptera; ecological factors have been claimed to be paramount. Yet, relevant quantitative studies investigating the role of ecological factors are lacking. We examined the influence of ecological factors on reproductive tactics in the drywood termite, Cryptotermes secundus. In this species, caste development is very flexible, with individuals having the option to remain at the natal nest as helpers/workers or to develop into dispersing reproductives (sexuals). An important ecological factor expected to influence this "decision" is food availability; C. secundus nests in a piece of wood that serves as food and shelter, with individuals never leaving the nest to forage. Thus, a reduction in the amount of food parallels a reduction in the nests' longevity. Therefore, we tested the influence of food availability on caste-developmental decisions in natural colonies, as well as in two experiments in which we simulated a gradual and a sudden decline in the amount of available food. In all trials dispersing sexuals occurred more often in colonies with diminished food resources than in colonies with abundant suitable food. Thus, regardless of how food declines, individuals seem to switch their tactic from being a helper to becoming a dispersing reproductive if nest conditions deteriorate and the nests's longevity decline.
Key words: eusocial insects, evolution, food availability, termite.
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INTRODUCTION |
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Hamilton's inclusive fitness concept (1964) has revolutionized our understanding of the evolution of altruistic behavior in which individuals forego personal reproduction to help other individuals reproduce. The general idea is that reproductive altruism may be favored when it is directed toward relatives because this allows indirect propagation of copies of the altruist's genes (inclusive fitness, Hamilton, 1964
; kin selection, Maynard Smith, 1964). Thus, altruistic behavior is favored if the benefits to the recipient weighed by relatedness are higher than the costs to the altruist. Extreme altruistic behavior is best known from eusocial insects. In Isoptera and Hymenoptera, such as ants, eusocial bees, and wasps, individuals permanently forego their own reproduction for helping others. The Hymenoptera have a haplodiploid sex determination that can result in relatedness asymmetries, with higher relatedness between full sisters than between mothers and their offspring; these relatedness asymmetries lead to intensive studies of testing theories on social evolution in this order. In contrast, termites have been rather neglected and are mentioned only briefly in major references on social evolution (Alexander, 1974; Bourke and Franks, 1995; Crozier and Pamilo, 1996; Keller, 1993; Lin and Michener, 1972). However, as termites and Hymenoptera show fundamental differences in their biology, different factors are likely to be the driving forces in the evolution and maintenance of eusociality in termites (Shellman-Reeve, 1997; Thorne, 1997).
In the diploid termites, no relatedness asymmetries per se exist that would favor altruistic helping for personal reproduction. Mechanisms that have been postulated to create relatedness asymmetries in termites, such as cyclical inbreeding (Bartz, 1979) or chromosomal translocations to the y-chromosome (Lacy, 1980; Luykx and Syren, 1979; Roisin, 2001), seem to be mainly theoretical speculations with limited relevance to the evolution of altruistic behavior (for cyclical inbreeding: Atkinson and Adams, 1997; Husseneder et al., 1999; Myles and Nutting, 1988; Shellman-Reeve, 2001; Thompson and Herbert, 1998; for chromosomal translocations: Crozier and Luykx, 1985; Leinaas, 1983; Roisin, 2001). Other factors, such as ecological pressures that increase the benefits and reduce the costs of helping, have been claimed to be paramount in favoring and maintaining kin-based altruism in termites (Myles, 1988; Roisin, 1999; Shellman-Reeve, 1997; Thorne, 1997). However, to our knowledge, no relevant study exists that investigated and tested the importance of such ecological factors for the expression of helping behavior in termite colonies (Lenz, 1994; Lenz et al., 1985).
In the present study, we investigate the importance of ecological factors for the maintenance of altruistic worker behavior in the model species Cryptotermes secundus (Hill) (Kalotermitdae). This termite is especially suited for such studies. As a "one-piece type" termite (i.e., a species that spends its entire colony life in a single piece of wood that serves both as shelter and as food; Abe, 1987; hereafter OP-termite) it does not have a true worker caste. The tasks of the workers are performed by late instar larvae and young nymphs that retain the potential to develop into reproductives. These workers can, therefore, be regarded as equivalent to helpers described in cooperatively breeding bird and mammal species (Brown, 1987; Emlen, 1991). So in accordance with the method of Roisin (2000), they will be called helpers hereafter. These helpers have often been called pseudergates. However, as pseudergates were defined as individuals that molted regressively (Grassé and Noirot, 1947), we avoid this ambiguous term. This flexibility in caste development in OP-termites contrasts with the "multiple-pieces type" termites (Lenz, 1994; multiple-site and central-site nester species, sensu Abe, 1987; hereafter MP-termites) that spend their colony life in a well-defined nest location, separated from the foraging sites. They have a true, that is, morphologically differentiated, worker caste with a reduced potential to reproduce, either as a neotenic or alate (Noirot, 1990; Roisin, 1999, 2000). The developmental flexibility of individuals of OP-termites to become either a helper or a dispersing alate shows that their development is less constrained than that of true workers in MP-termites. Therefore, it is expected that the maintenance of altruistic behavior is still under active selection and that factors influencing the expression of such behavior can be studied in extant OP-termites such as C. secundus.
The greater developmental flexibility of individuals of OP-termites compared with MP-termites may be in direct response to their more uncertain environment (see also Higashi et al., 1991): the site originally colonized by the founding reproductives is the sole food source for the colony. Therefore, initially the colony has high food abundance, but this finite resource decreases with colony age, eventually resulting in a food shortage and nest instability (see also La Fage and Nutting, 1978; Lenz, 1976, 1994; Lenz et al., 1985). This scenario presents a challenge to the maintenance of altruistic behavior (Higashi et al., 1991). Yet, the importance of resource availability in shaping termite societies has been given insufficient consideration (Lenz, 1994; Watson and Sewell, 1985). Therefore, we targeted the role of food availability among the many ecological factors that could influence the decision to become a helper or a dispersing sexual. We tested whether food abundant colonies differed from food limited colonies in the occurrence and number of dispersing sexuals produced: first, in natural colonies from the field and, second, in two experiments simulating either a gradual or a sudden decline in food availability.
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METHODS |
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Study site
The study was conducted in a mangrove area near Palmerston-Channel Island in Darwin Harbor, Northern Territory, Australia (12°30' S 131°00' E). The mangrove community is typical for this region, with a high diversity of more than 30 species of trees (Wightman, 1989
). There is a clear zonation of the main mangrove tree species with 2–5 m tall Ceriops tagal near the dry edge of the mangroves (Hutchings and Saenger, 1987). C. secundus occurs in dead C. tagal trees within that zone (Miller and Paton, 1983).
Natural colonies
C. tagal trees occur in patches of trees of similar height. Only dead trees higher than 2 m were infested by C. secundus (data not shown). All dead trees were removed from three neighboring C. tagal patches that were separated by distances of 300 to 1000 m. Together these three patches covered an area of about 0.2 x 1.4 km. In total about 1000 logs with more than 400 C. secundus colonies were collected from 1999–2001.
We brought whole dead trees from the field site to the laboratory, where they were carefully dissected with a hammer and chisel. If we found C. secundus, we assessed food availability by visual inspection of the dead tree and the galleries therein; if logs were hollowed out and galleries extended to the outer layers of the log, we designated the colonies as natural-food-limited colonies. Other colonies were designated as natural-food-abundant colonies. All termites of a colony were extracted by hand and the colony composition determined. We distinguished between eggs, larvae (individuals up to the third instar that do not perform colony tasks and need to be fed; data not shown), helpers (individuals from the fourth instar onward with the exception of late stage nymphs and soldiers), soldiers (individuals with a phragmotic head), late stage nymphs (individuals with large obvious wing buds), alates (winged sexuals), and primary and secondary (neotenic) reproductives. Penultimate and ultimate nymphs (i.e., the last two stages in the development towards alates) and alates were counted as dispersing sexuals. It was necessary to include these last two stages before the imaginal molt because development of alates was not completely synchronized; these nymphs and alates were present from April–mid August, when nuptial flights begin.
Experiments
We used natural colonies with two primary reproductives for experiments. They were collected, as described above, from January–March, and colony composition was determined. Individuals were transferred to Pinus radiata wood blocks, which are commercially available and can be standardized in form and size to adjust to colony size and experiment (see below). Earlier experiments showed that the development of colonies did not differ between natural C. tagal and P. radiata wood (data not shown).
We performed two experiments; in one experiment, food availability declined gradually reflecting the progressive exploitation during a colony's lifetime, and the second experiment simulated a sudden decline in food availability as it occurs when parts of dead trees break during thunderstorms or cyclones which are common in the study region. The second experiment was done in the field, and the first experiment had to be performed in the laboratory as the set up in the field failed when heavy thunderstorms washed the wood blocks away. However, comparison of abundant-food colonies under both conditions allowed to control for potential laboratory artifacts.
Gradual decline in food availability: laboratory experiments
Experimental colonies were established in wood blocks using a ratio of one termite for at least 10 cm3 of wood volume, thus providing an abundant food supply (for details, see Table 1; Lenz, 1994); food availability was manipulated by varying the time the termites were kept in these wood blocks: (1) for colonies with abundant food (hereafter gradual-food-abundant colonies) 56 infested blocks were stored in the laboratory under standard conditions that are appropriate for C. secundus (Lenz, 1994) for about 1.5 years. Thus, these colonies were collected prior to the swarming period of the next year when suitable food was still abundant and galleries did not extend to the wood surface. (2) For colonies with limited food (hereafter gradual-food-limited colonies) 36 infested blocks were stored as in (1); however, they were only collected prior to the swarming period after 2.5 years when the blocks were substantially eaten so that the galleries extended to the outer layers of the blocks.
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Sudden decline in food availability: field experiments
In this experiment, food availability was manipulated by varying the size of the wood blocks where the termites were housed: (1) 19 colonies with abundant food (hereafter sudden-food-abundant colonies) were set up in wood blocks using the abundant food ratio of one termite for at least 10 cm3 of wood volume (see above, Table 1); and (2) 16 colonies with limited food (hereafter sudden-food-limited colonies) were set up in wood blocks that measured 25% that size (i.e., one termite for 2.5-cm3 wood). All infested P. radiata blocks were brought to the field to the same position where C. secundus had been collected. The blocks were attached to C. tagal trees and covered with flat plastic lids to prevent complete soaking during monsoonal rains. All colonies were collected before the swarming period of the next year (i.e., after approximately 1.5 years).
For all experiments after collection, the wood blocks containing the experimental colonies were dissected and the colony composition determined. As in the natural colonies, all collections were made before the first nuptial flights occurred, and penultimate and ultimate nymphs and alates were counted as dispersing sexuals.
Statistical analysis
First, we compared food-limited colonies to food-abundant colonies, separately for all trials. We tested frequency tables of the occurrence (yes, no) of dispersing sexuals with chi-square contingency analysis; for significant differences we calculated the risk ratio with 95% confidence intervals (Norusis, 1993). The number of dispersing sexuals produced were analyzed with general linear models, with food availability as between-subject factor and colony size at the end of the experiment as covariate. Therefore, data were checked for assumptions of parametric tests by histogram plots and Kolmogorov Smirnov tests. Log-transformations were used to reasonably approximate normal distributions of the data (Sokal and Rohlf, 2000).
Second, to test for artifacts of handling (natural/experiment) and location (field/laboratory), we compared sudden-food-abundant colonies (field experiment), respectively, with natural-food-abundant colonies and with gradual-food-abundant colonies (laboratory experiments). Again, the occurrence of dispersing sexuals was tested with chi-square contingency analysis. The number of sexuals could not be analyzed owing to low sample sizes of sudden-food-abundant colonies with sexuals. For nonsignificant differences, a power analysis for contingency tables was performed with GPOWER, a freeware software package (Faul and Erdfelder, 1992). A similar comparison for food-limited colonies or a multicomparison approach using food availability and handling/location as between subject factors in a general linear model was not performed; the power of such analysis would have been too low (owing to small sample sizes of some groups) to draw reliable conclusions from nonsignificant effects.
All analyses, with the exception of the power analysis, were performed with SPSS 10.0. If several tests were performed on the same data set, we adjusted the probability values by using Bonferroni correction.
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RESULTS |
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Natural colonies
The frequency of the occurrence of dispersing sexuals was significantly higher in natural-food-limited than in food-abundant colonies (contingency analysis:
= 5.37, p =.021) (Figure 1a). In natural-food-limited colonies, five out of five colonies had sexuals (100%), whereas the corresponding values for natural-food-abundant colonies were 58 out of 123 colonies (47.2%). Thus, according to the risk ratio, it was 2.1 times (c.l. 1.76–2.56) more likely that a natural-food-limited colony had sexuals than did a natural-food-abundant colony. In both natural food-abundant and food-limited colonies, the number of dispersing sexuals increased with colony size (i.e., number of helpers; ANOVA: F1,42 = 16.19, p <.001) (Figure 1a). When controlling for colony size, food-limited colonies had significantly more dispersing sexuals than did food-abundant colonies (ANOVA: F1,42 = 6.78, p =.013).
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Gradual decline of food availability: laboratory experiments
Gradual-food-limited colonies had significantly more often dispersing sexuals than did gradual-food-abundant colonies (contingency analysis:
= 10.33, p =.001) (Figure 1b). In gradual-food-limited colonies, 21 out of 36 colonies produced sexuals (58.3%), whereas the corresponding values for gradual-food-abundant colonies were 14 out of 56 colonies (25.0%). The risk ratio to have sexuals for gradual-food-limited colonies was 2.3 times (c.l. 1.37–3.96) that for a gradual-food-abundant colonies. If colonies produced dispersing sexuals, there was a trend for gradual-food-limited colonies to have more sexuals than did gradual-food-abundant colonies (ANOVA: F1,35 = 3.50, p =.070), whereas colony size had no influence on the number of sexuals (ANOVA: F1,35 = 0.01, p =.927) (Figure 1b). Note the smaller colony size range in this experiment compared with the natural colonies (Figure 1a,b).
Sudden decline of food availability: field experiments
Sudden-food-limited colonies had significantly more often dispersing sexuals than did sudden-food-abundant colonies (contingency analysis: = 8.12, p =.004) (Figure 1c). In sudden-food-limited colonies, 10 out of 16 colonies had sexuals (62.5%), whereas the corresponding values for sudden-food-abundant colonies were three out of 19 colonies (15.8%). Thus, it was 3.9 times (c.l. 1.31–11.96) more likely that a sudden-food-limited colony had sexuals than did a sudden-food-abundant colony. Because of the low number of food-abundant colonies with dispersing sexuals, a further comparison of the numbers of sexuals was not possible. Note the smaller colony size range in this experiment compared with the natural colonies (Figure 1a,c).
Comparison between natural and experimental field colonies: artifact of handling
As colony size had an influence on the production of dispersing sexuals in natural colonies (see above) and natural colonies were much larger than experimental field colonies (i.e., sudden decline experiment; maximal colony size: 1400 individuals versus 100 individuals) (Figure 1a,c), this analysis was restricted to colonies with a maximum of 100 individuals. The occurrence of dispersing sexuals did not differ significantly between natural- and sudden-food-abundant colonies (contingency analysis: = 1.42, p =.233). The power of rejecting the wrong null hypothesis was 0.679.
Comparison between field and laboratory experiments: artifact of location
The occurrence of dispersing sexuals did not differ significantly between the food-abundant laboratory experiments (i.e., gradual-food-abundant colonies) and food-abundant field experiments (i.e., sudden-food-abundant colonies; contingency analysis: = 1.06, p =.304) (Figure 1b,c). The power for rejecting the wrong null hypothesis was 0.503.
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DISCUSSION |
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Food availability influenced the number of dispersing sexuals being produced. Natural as well as gradual- and sudden-decline experimental colonies produced more often sexuals when food was diminishing than when food was abundant. Furthermore, the handling of the termites in the experiments and the location of the colonies either in the field or in the laboratory did not produce artifacts as comparison of the food-abundant colonies showed. The only difference was the lack of a correlation between colony size and the number of sexuals being produced in gradual decline colonies while such a correlation occurred in natural colonies. This difference can be explained by the larger range of colony sizes in the natural colonies compared with the experimental colonies (Figure 1a,b). Thus, all results suggest that food limitation shifts the tactic of individuals from helpers to sexuals. Preliminary behavioral and developmental observations show that there are three types of helpers (data not shown): (1) individuals that are still too young to proceed toward the sexual stage in the next swarming season, (2) individuals that can reach the sexual stage in the next swarming season for the first time, and (3) individuals that could have reached the sexual stage already during the previous swarming season, but that delayed their dispersal by regressive molts from nymphs with obvious wing buds to stages with small or no wing buds (i.e., pseudergates; sensu Grassé and Noirot, 1947
). The last type of individuals seem to represent those that "abandon" the helper role when food resources decline but might stay when food is abundant. In contrast to wing pad mutilations by nest mates mentioned in former studies (Myles, 1986; Roisin, 1994; Zimmerman, 1983), no aggressive manipulations by siblings or parents were observed under either food condition in this study.
The importance of food availability and nutrition on caste determination in termites has long been discussed (Buchli, 1958; La Fage and Nutting, 1978; Lenz, 1976, 1994). However, many examples are anecdotal and as La Fage and Nutting (1978) pointed out, relevant information is sketchy and in many cases based on circumstantial evidence. A noticeable exception is a study on Cryptotermes species in which food availability was manipulated (Lenz, 1994). However, this study has the drawback that it was not carried out with whole colonies, but groups set up from brachypterous nymphs. Nevertheless, as in the current study, when food was in more limited supply, subcolonies of C. cynocephalus and C. queenslandis produced more dispersing sexuals as more individuals proceeded to becoming alates (see also reports on some other OP-termites and the reproduction of Kalotermes flavicollis colonies in the laboratory; Lenz, 1976). This switch in development is adaptive from the helpers' point of view. They should try to leave the nest, when nest conditions deteriorate and the chances to raise further siblings or inherit the colony are low. In OP-termites, such as C. secundus, helpers have the potential to respond to resource availability by developing into dispersing alates. This is less possible in MP-termites that have true workers with reduced developmental flexibility and might explain why Reticulitermes santonensis (a MP-termite) retards the production of dispersing sexuals when nest conditions deteriorate (Buchli, 1958). Thus, the present results demonstrate for entire colonies that helpers of OP-termites "adjust" their development to food availability and abandon the helper role when food resources in the natal nest decline. At this point there is still a considerable amount of food left and there are no signs of starvation in the termites (e.g., the accumulation of uric acid), so helpers still have enough food to develop into sexuals.
These results might also indicate that the decision to abandon the nest is under self-control. In many social Hymenoptera, caste fate is often socially controlled, probably owing to the dependence of the young (Bourke and Ratnieks, 1999; Reuter and Keller, 2001). In C. secundus, the individuals are rather independent when caste fate is determined (in contrast also to MP-termites), so a situation exists similar to that of Melipona stingless bees. This is an exceptional Hymenopteran genus in which queens and workers are of the same size and are reared from the same types of mass provisioned cells, allowing any individual to decide for itself whether to become a queen or a worker (Ratnieks, 2001). However, in contrast to Melipona, in which considerable conflict about caste fate exists, in C. secundus it also seems to be in the interest of the reproductives that helpers leave the nest and no aggressive manipulations were observed. As reproductives are generally thought to proximately regulate the development of sexuals in termites (Lüscher, 1974; Stuart, 1979), their regulation probably functions as a signal (pheromonal queen signal; sensu Keller and Nonacs, 1993); that is, helpers react to the reproductives signals in ways that increase their (and possibly the reproductives') inclusive fitness. However, more research on proximate and ultimate causation is necessary to address the topic of caste regulation in termites adequately.
The flexibility of caste development poses also questions on other proximate causes: how does C. secundus assess food availability? The tunnel system can provide a direct measurement of food availability, although some instances indicate that ultrasonic acoustic emissions produced by chewing might also be important (Lenz, 1994). Changes in caste differentiation might be indirect responses owing to changes in the level of interactions and the rate of trophallactic exchange between colony members as the tunnel system extends (Lenz et al., 1985). Also here, more studies are needed to address this question in detail.
Conclusions
Being a helper, at least in Cryptotermes and probably in most OP-termites, is not a lifetime strategy, but a very flexible tactic that depends on environmental conditions. The choice between the tactics seems to be influenced by food availability and, therefore, the future stability and residual longevity of the natal nest, as is shown for the first time in our experiments with whole colonies. In contrast to monogamous Hymenoptera, relatedness is unlikely to influence the choice between both tactics, as the average relatedness coefficient to all offspring is 0.5 for both tactics in these monogamous colonies. However, clearly more studies are necessary to evaluate these alternative tactics. Such studies should investigate other cost and benefit factors such as the direct benefit that helpers can gain by becoming a neotenic replacement reproductive in the natal nest or the costs of dispersal and own colony foundation.
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ACKNOWLEDGEMENTS |
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We thank L. Miller and the Tropical Ecosystems Research Center of CSIRO in Darwin for support in Australia, V. Salewski for collecting and splitting termite colonies, S. Runko for organizing the P. radiata blocks, and C. Anderson, K. Boomsma, T. Evans, J. Heinze, B. Peters, Y. Roisin, E. Strohm, and an anonymous referee for helpful comments on the manuscript. The project was supported by the German Science Foundation (KO 1895/1-1, KO 1895/2-1). The experiments comply with the current laws of Australia where they were performed.
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