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Is the Aestivation of the Earthworm Hormogaster Elisae a Paradiapause?

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Is the Aestivation of the Earthworm Hormogaster Elisae a Paradiapause? Invertebrate Biology 125(3): 250–255. Journal compilation r 2006, The American Microscopical Society, Inc. No claim to original Complutense University of Madrid works. DOI: 10.1111/j.1744-7410.2006.00057.x Is the aestivation of the earthworm Hormogaster elisae a paradiapause? Darı´oJ.Dı´az Cosı´n,a Marı´a Pilar Ruiz, Marta Ramajo, and Mo´nica Gutie´rrez Departamento de Zoologı´a y Antropologı´aFı´sica, Facultad de Biologı´a, Universidad Complutense, 28040 Madrid, Spain Abstract. We report the results of a laboratory study of the aestivation of Hormogaster elisae to determine the nature of the inactive period (diapause or quiescence) and to evaluate the influence of soil moisture, temperature, season, and earthworm body weight on the process. The results showed that specimens of H. elisae underwent facultative diapause—paradia- pause—characterized by the construction of aestivation chambers in which the animal coils up and its activity decreases. Soil moisture appeared to be the most important environmental factor involved in the onset of aestivation. Temperature and time of year also had some influence, but earthworm body weight appeared to have none. Aestivating earthworms showed a decrease of 41.6% in mean body weight. Once replaced in soil with 20% moisture content, they took 6.473.1 d to exit their chambers and another 6.573.6 d to recover their initial body weight. Additional key words: earthworms, aestivation chambers, diapause, quiescence When environmental conditions are too severe for or temperature; this response ends as soon as condi- normal activity to continue, earthworms can react in tions become favorable. In quiescence, earthworms different ways. For example, when soil moisture stop feeding and remain in a torpid state, but they do content is inadequate, they can move vertically or not make special chambers. Bouche´(1972) distin- horizontally, form cocoons, or modify their metabo- guished three types of quiescence: anhydrobiosis, lism to reduce water loss, entering into what is known reaction to toxicity, and hibernation. The latter is as a ‘‘resting state,’’ ‘‘dormant stage,’’ or ‘‘state of initiated when temperatures fall below 21–41C. The inactivity’’ (Lee 1985; Edwards & Bohlen 1996). This worms coil up in small soil spaces just below the reduction in metabolic activity has been described in superficial frozen soil layer. Lee (1985) indicates that the literature as either diapause (obligatory or facul- the differences between obligatory and facultative tative) or quiescence (Satchell 1967; Nordstro¨m& diapause and quiescence can be site specific and Rundgren 1974). It has been suggested that obliga- that a gradation exists between these processes with tory diapause might be controlled by neurosecretions variations in response to the severity of the stress (Lee 1985). The process begins at a certain time of the suffered by individual populations. Variations may year, and once underway its duration is independent be seen in the response of a species with respect to the of artificial manipulation of environmental factors. time of year; e.g., Scherotheca gigas rodana var. The earthworms stop feeding, empty their gut, and gallisiani BOUCHE 1972, an endogeic Mediterranean construct an aestivation chamber in which they re- species, undergoes diapause in summer and quies- main coiled up in a state of low activity (Michon cence in winter (Gallisian 1975). 1957; Saussey 1966). Facultative diapause, or para- As the majority of the available aestivation data diapause (Saussey 1966), is different from the obliga- come from field observations of lumbricids, of inter- tory type in that it may terminate at any time when est is a better understanding of the processes of environmental conditions become suitable for nor- inactivity in other families of terrestrial oligochaetes. mal activities. We studied a Mediterranean species, Hormogaster Quiescence is defined as a direct response to varia- elisae A´LVAREZ 1977 (Hormogastridae), an endogeic tion in an environmental factor such as soil moisture species endemic to the center of the Iberian Peninsula (Madrid and Segovia), found in soils poor in organic matter and whose habitat is subject to large varia- a Author for correspondence. tions in soil temperature and moisture over the year E-mail: [email protected] (strong summer drought). In response to moisture Aestivation in Hormogaster elisae 251 content, this species moves vertically and builds casts gÀ1 live earthworm mass per day; Dı´az Cosı´n aestivation chambers as deep as 50 cm in the soil et al. 1996). The microcosms at external temperature (Valle et al. 1997, 1999); e.g., we found aestivation were put on a window ledge, shaded by an outer chambers during a drought in May 2003 at El Molar. lattice window. Our aim was to determine, by means of laboratory The duration of the experiment was 2 weeks. experiments, the nature of the inactive period in this Moisture content was maintained by measuring the species and to evaluate the influence of soil moisture, weight change of the microcosms, and adding water temperature, season, and earthworm body weight on as necessary every 2–3 d. At the end of the experi- the process. ment, the microcosms were examined, and the num- ber of aestivating (pale, coiled into a tight ball in a mucus-lined chamber) and dead worms was counted. Methods The same procedure was repeated in May 2000 Soils and earthworms were collected during April (spring), June–July 2000 (summer), October–Novem- and October 2000, and April 2001 and 2002 at El ber 2000 (autumn), and February 2001 (winter). Molar (Madrid), UTM 30TVL5210, by manual ex- The chi-square of the G-test (calculated previously cavation and hand sorting. The worms were kept in using contingency tables) and log-linear analysis (em- the laboratory in the same soil (El Molar) until they ploying Statistica for Windows 4.5, Statsoft, Tulsa, were used for the experiments. Details of the soil, OK) were used to analyze the influence of soil moist- climate, and vegetation characteristics of El Molar ure, temperature treatment, season, and earthworm can be found in Garvı´n et al. (2000). weight class on the number of aestivating earthworms per microcosm. The G-test is appropriate to test the Seasonal cultivation combined influence of categorical variables. The log- linear analysis was used to search for a ‘‘good model’’ The earthworms were separated into three weight that includes the least number of interactions neces- classes: small (o1 g), medium (1–2 g), and large sary to fit the data. Temperature and season are (42 g) (this distribution was not an effort to describe interdependent variables; therefore, only temperature different life stages in the earthworms). Three differ- was used for the statistical analysis, or season using ent soil moistures (10%, 15%, and 20% water con- the data from the constant temperature treatment tent on a dry mass basis) and temperature treatments (181C, growth chamber) to detect whether there is (growth chamber, laboratory temperature, and ex- an ‘‘internal clock’’ that regulates the aestivation, ternal temperature) were combined for a total of nine independent of temperature variations. treatments. Each treatment was replicated 3Â , one for each weight class (27 microcosms in total). Additional experiments Growth chamber temperature was maintained at 181C. Laboratory temperatures during the study The results obtained suggested that further experi- period (averages of maximal and minimal) were ments might be undertaken to investigate the process 25.641C and 22.151C in spring, 29.21C and 25.471C more fully. The influence of temperature was com- in summer, 22.821C and 19.31C in autumn, and plemented by a second series of experiments with two 22.681C and 19.31C in winter. The averages of max- new temperatures (131Cand231C) in a culture imal and minimal external temperatures, which fluc- chamber. In May 2002, three different soil moistures tuated between day and night, were 28.31C and 7.11C (10%, 15%, and 20% water content on a dry mass in spring, 36.41C and 14.31C in summer, 17.91Cand basis) and two temperatures (131C and 231Cin 12.51C in autumn, and 11.81C and 4.61C in winter growth chambers) were combined for a total of six (Madrid, University City Weather Station). treatments, with three replicates of each treatment The microcosms consisted of plastic boxes con- (18 microcosms in total). Each microcosm consisted taining 2-mm sieved soil, from the collection site, of a plastic box containing 650 g of air-dried soil, adjusted to the desired moisture. Three earthworms sieved at 2 mm and adjusted to the desired moisture of the same weight class were introduced into each content. Three earthworms, without separation in microcosm (81 earthworms in total). The quantity of weight class (or of different size), were introduced dry soil used (400 g for small earthworm microcosms into each microcosm (54 earthworms in total). and 650 g for medium and large ones) was adequate The duration of the experiment was 2 weeks and to prevent food from becoming a limiting factor to moisture content was maintained by adding water as activity. This quantity was calculated from the mean necessary every 2–3 d. At the end of the experiment, cast production rate for this species (3.34 g dry the microcosms were examined and the number of Invertebrate Biology vol. 125, no. 3, summer 2006 252 Dı´az Cosı´n, Ruiz, Ramajo, & Gutie´rrez aestivating worms was counted. The G-test (employing above. Earthworms were weighed and one was Statistica for Windows 4.5) was used to analyze the placed in each microcosm. The duration of the ex- combined influence of soil moisture and temperature on periment was 4 months (May–September 2001). The the number of aestivating earthworms per microcosm. moisture content was maintained constant by adding In June–July 2002, a third series of experiments water as necessary every 7–10 d.
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