High metabolic and water-loss rates in caterpillar aggregations: evidence against the resource-conservation hypothesis

Schoombie, Ruben E.; Boardman, Leigh; Groenewald, Berlizé; Glazier, Douglas S.; Daalen, Corné E. van; Clusella‐Trullas, Susana; Terblanche, John S.

doi:10.1242/jeb.095554

Cited by 12 publications

(14 citation statements)

References 11 publications

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“…Alternatively, hypometric mass-scaling of metabolism may be determined by variation in demand for ATP [28][29][30] caused by size-based selection for the performance of specific behaviours affecting metabolism [31][32][33][34][35], or from a mixture of mechanisms that vary across species [23,35]. These alternatives present different and often competing theoretical views of allometric scaling.…”

Section: Introductionmentioning

confidence: 99%

“…However, homeothermic, cold-exposed groups may be a special case because the surface area : volume ratio directly affects the balance of heat loss to heat production; it is difficult to expand such considerations to social groups such as ant colonies that do not endothermically thermoregulate. Among non-social and ectothermic insects, changing group size does not affect the metabolic rate of aggregating caterpillars [28,65]. Experimental tests of size effects have also been conducted by manipulating the size of modular colonial marine organisms [1,31,33,35].…”

Section: Introductionmentioning

confidence: 99%

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Differentiating causality and correlation in allometric scaling: ant colony size drives metabolic hypometry

et al. 2017

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Metabolic rates of individual animals and social insect colonies generally scale hypometrically, with mass-specific metabolic rates decreasing with increasing size. Although this allometry has wide ranging effects on social behaviour, ecology and evolution, its causes remain controversial. Because it is difficult to experimentally manipulate body size of organisms, most studies of metabolic scaling depend on correlative data, limiting their ability to determine causation. To overcome this limitation, we experimentally reduced the size of harvester ant colonies (Pogonomyrmex californicus) and quantified the consequent increase in mass-specific metabolic rates. Our results clearly demonstrate a causal relationship between colony size and hypometric changes in metabolic rate that could not be explained by changes in physical density. These findings provide evidence against prominent models arguing that the hypometric scaling of metabolic rate is primarily driven by constraints on resource delivery or surface area/volume ratios, because colonies were provided with excess food and colony size does not affect individual oxygen or nutrient transport. We found that larger colonies had lower median walking speeds and relatively more stationary ants and including walking speed as a variable in the mass-scaling allometry greatly reduced the amount of residual variation in the model, reinforcing the role of behaviour in metabolic allometry. Following the experimental size reduction, however, the proportion of stationary ants increased, demonstrating that variation in locomotory activity cannot solely explain hypometric scaling of metabolic rates in these colonies. Based on prior studies of this species, the increase in metabolic rate in sizereduced colonies could be due to increased anabolic processes associated with brood care and colony growth.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Differentiating causality and correlation in allometric scaling: ant colony size drives metabolic hypometry

et al. 2017

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“…Lack of a group effect with regard to water loss in C. mesochoreus is different from the enhanced water conservation attributes of grouping behavior in nematodes (Wharton 1996) and also hairworms (Yoder et al 2014). Not all invertebrates retain water more effectively by forming aggregations through group effects: none was observed in caterpillars (Schoombie et al 2013). Our results on C. mesochoreus extend Schoombie et al's (2013) trend to include a branchiobdellidan and a physiological correlation that links lack of a resource-conservation group effect with extremely high rates of water loss by the organism.…”

Section: Discussionmentioning

confidence: 90%

“…Not all invertebrates retain water more effectively by forming aggregations through group effects: none was observed in caterpillars (Schoombie et al 2013). Our results on C. mesochoreus extend Schoombie et al's (2013) trend to include a branchiobdellidan and a physiological correlation that links lack of a resource-conservation group effect with extremely high rates of water loss by the organism. Aggregation itself could be beneficial for reasons other than maintaining water balance, such as sex, access to graze on benthic substrate and avoidance of removal from host grooming (Brown et al 2002;Gelder and Williams 2011).…”

Section: Discussionmentioning

confidence: 99%

Hygric stresses and strategies in maintaining the association between crayfish and ectosymbiotic worms across vastly different environments

et al. 2016

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Crayfish and their ectosymbiotic worms may be a valuable model system for studying strategies to maintain symbiotic relationships strained by host-induced environmental shifts. Ectosymbiotic branchiobdellidan worms are thought to be dependent on crayfish hosts for reproduction. However, many crayfish species leave surface waters to excavate and reside in subterranean burrows. During this semi-terrestrial phase, crayfish are frequently out of water, subjecting their associated worms to desiccation. Water balance characteristics of Cambarincola mesochoreus, an ectosymbiont of Procambarus clarkii, were examined to elucidate strategies for surviving emersion while maintaining host associations. Emersed worms were characterized by a high water loss rate and low tolerance for dehydration. A lack of direct water contact eventually prompted a coiled, immobile dormant state where water loss was temporarily suppressed. This dormant state was broken by addition of water and re-entered by subsequent emersion. Neither group effects by clustering of many worms, nor water vapor absorption were utilized as mechanisms to increase desiccation hardiness. When crayfish leave surface or subterranean water, worm survival while maintaining host contact is likely facilitated by facultative quiescence. However, this strategy only allows for survival during relatively short-term, cyclic bouts of emersion. Survival of longer-term emersion periods would require worms to leave hosts and remain behind in surface or subterranean water. These strategies likely incur counterbalancing trade-offs: increased mortality but maintenance of host association versus increased survival but temporary or permanent loss of host association and sites for reproduction.

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“…Aggregation, whether social or not, is most likely a mechanism for body water conservation in many invertebrate groups. Examples of this phenomenon are found in Mollusca (Cook, ; Chapman & Underwood, ; Rojas et al , ); Tardigrada (Ivarsson & Jönsson, ); Acari (Glass et al , ; Benoit et al , ); Insecta, as in fly maggots (Rivers et al , ), caterpillars (Klok & Chown, , Schoombie et al , ), beetles (Yoder et al , ; Rasa, ; Yoder & Smith, ; Benoit et al , ), crickets (Yoder et al , ) and cockroaches (Yoder & Grojean, ; Dambach & Goehlen, ); and in certain semiterrestrial crabs (Yoder et al , ). However, few of these studies have investigated the relationship between water losses and the size of the groups thoroughly; special attention has only been directed at small groups and at low density values.…”

Section: Introductionmentioning

confidence: 99%

Effects of group size on aggregation against desiccation in woodlice (Isopoda:Oniscidea)

et al. 2014

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Aggregation in terrestrial isopods, a behaviour that results in the formation of dense clusters, is readily accepted as a mechanism of resistance to desiccation. Thus, aggregation is considered to be an adaptation to terrestrial life in this fully terrestrial suborder of crustaceans. In the present study of Porcellio scaber Latreille, a cosmopolitan species, individual water loss is investigated experimentally as a function of the size of the aggregates and, for the first time, over a large range of group sizes (groups of 1, 10, 20, 40, 60, 80 and 100 individuals). From the perspective of an isolated individual, aggregation behaviour is effective in reducing the rate of water loss whatever the group size, and reduces the individual water loss rate by more than half in large groups. However, the water loss rate of an individual follows a power law according to group size. Accordingly, if the addition of individuals to small groups strongly reduces the water losses per individual, adding individuals to large groups only slightly reduces the individual water losses. Thus, the successful reduction of the water loss rate by this aggregation behaviour is confirmed, although only up to a certain limit, particularly if the number of individuals per aggregate exceeds 50–60 under the experimental conditions used in the present study. Moreover, the individual surface area exposed to the air, as a function of group size, follows a similar pattern (i.e. a similar power law). Thus, a geometrical explanation is proposed for the nonlinear water losses in woodlice aggregates. These results are discussed in relation to the group sizes observed both in the laboratory and the field.

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High metabolic and water-loss rates in caterpillar aggregations: evidence against the resource-conservation hypothesis

Cited by 12 publications

References 11 publications

Differentiating causality and correlation in allometric scaling: ant colony size drives metabolic hypometry

Differentiating causality and correlation in allometric scaling: ant colony size drives metabolic hypometry

Hygric stresses and strategies in maintaining the association between crayfish and ectosymbiotic worms across vastly different environments

Effects of group size on aggregation against desiccation in woodlice (Isopoda:Oniscidea)

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