The Influence of Temperature on the Development Time of Three Oribatid Mite Species (Acari, Oribatida)

Studies on the development of oribatid mites are an important aspect in acarology. The ontogeny and the duration of development for these animals have usually been unsufficiently investigated. The data, even if available in the literature, are not always suitable for comparison and interpretation. The problems are caused by the use of various cultivation techniques (Shaldybina 1969а, Seniczak 1972), lack of recorded lengths of development for separate stages (Harten- stein 1962, Block 1965) or unavoidable fluctuations of air temperature (Weigmann 1975). Moreover, it is generally known that environmental factors (tempe North-West J Zool, 4, 2008 Oradea, Romania rature, soil acidity, humidity, amount and quality of food, disturbances) and the density of other microarthropods can partly affect the development duration of moss mites (Shaldybina 1969b, Siepel 1994, Maraun & Scheu 2000, Uvarov 2003). However, the largest influence on the generation time is that of the genetic mode of the order or family. Siepel (1994) noted that all variations in development time caused by the environment are smaller than variations within families or order. The problems with developmental studies may be caused by the reproduction mode of moss mites. It is assumed that the generation time of parthenogens is shorter than that of sexual species (Ghilarov 1982, Ryabinin & Pan΄kov 1987). However, data about relationship between

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generation time and mode of reproduction are rare (Norton & Palmer 1991). Nevertheless, it is generally known that oribatid mites have low metabolic rates, slow development low fecundity, low number of eggs and juvenile survival, so they exemplify the "K-selected" organisms (MacArthur & Wilson 1967, Crossley 1977). The development duration from egg to adult may vary from several months to two years in temperate forest soils (Luxton 1981) and the generation time at 18 ºС may take from 33 days in Oppia concolor (Nannelli 1975) to 400 days in Steganacarus magnus (Webb 1977). However, in warmer climates the number of generations per year may be very high (Norton & Palmer 1991). Cool climates prolong the life cycles of moss mites. It has been shown that Tectocepheus velatus (Michael 1880) from northern Norway lives two or more years (Solhøy 1975) and the duration of nymphal stages of the Antarctic species Alaskozetes antarcticus (Michael 1903) may be more than three years (Burn 1986). Recently, the development duration of Scutovertex rugosus Mihelcic, 1957 and S. perforatus Sitnikova, 1975 was investigated at two temperatures (Ermilov et al. 2008). Similarly, the authors observed considerable differences that indicated a longer life cycle at lower temperatures. Fourteen species of Ceratoppia genus and 34 species of Nanhermannia genus have been described so far (Subías 2004). In Russia, nine species of Сeratoppia and eleven species of Nanhermannia genus have been recorded. However, only four species are widespread in the European part of Russia (the Nizhniy Novgorod region): N. nana (Nicolet, 1855), N. coronata Berlese, 1913, Ceratoppia bipilis (Hermann, 1804) and C. quadridentata (Haller, 1882). So far, the data on development duration have concerned two species only: C. bipilis and N. nana (Sengbusch 1958, Krivolutsky 1995, Ermilov 2004, Michael 1884-1888). The aim of this paper is to examine and compare the development time of two sexual species from the family Ceratoppiidae: Ceratoppia bipilis (Hermann, 1804) and C. quadridentata (Haller, 1882) and one parthenogenetic Nanhermannia cf. coronate Berlese, 1913 (Nanhermanniidae) with the earlier studied parthenogenetic species N. nana (Nicolet, 1855). The cultivation of the studied species was carried out in laboratory under 100% humidity, at two temperatures and with the surplus of food.

quadridentata – in 2004 (experiment at 20˚C) and 2006 (17˚C), and on N. cf. coronata – in 2005-2006 (experiment at 22.5˚C) and 2007 (experiment at 20˚C). The cultures were started in March and April. All juvenile and adult specimens were collected in biotopes in the Nizhniy Novgorod region (Russia) by Dr. M.P. Chistyakov and Dr. S.G. Ermilov. The species were collected from the European part of Russia, i.e. the Nizhniy Novgorod region, northwest of Nizhniy Novgorod city. Ceratoppia species and Nanhermannia cf. coronata were collected from soil, moss and detritus of the Kozinskiy pine forest (Balachninskiy district). Groups of adult specimens were cultured in plastic boxes, larvae and nymphs in culture chambers. The experiment was carried out in a surplus of food, 100% humidity and at two temperatures: 17ºС and 20ºС for Ceratoppia species and 20ºС and 22.5ºС for Nanhermannia. Exicators with boxes and chambers were covered with light-proof covers and placed in thermal cases. Because of different places of sampling, mites were fed with varied food: pleurococcal algae (Pleurococcus sp.), parts of lichens (Cladonia silvatica and Cetraria islandica) and raw potato. The cultivation technique and calculations follow instructions of Sitnikova 1959, Shaldybina 1969а and Ermilov 2006. Calculations of the lower temperature threshold for development, the sum of effective temperatures and theoretical duration of development of mites follow methods presented by Chistyakov 1970 and Ermilov et al. 2004.

All adult specimens of C. bipilis ate because the development of studied species was measured at two temperatures, there was an opportunity to calculate theoretical duration of develop- ment (n), following the equations of Chistyakov (1970) and Ermilov (2004): X - the sum of effective temperatures Т – the ambient temperature during development C – the lower temperature threshold for development. The sum of effective temperatures was calculated as:

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t – number of days when the temperature exceeded the development threshold The lower development threshold temperature was calculated as: As a result: mainly pleurococcal algae (Pleurococcus sp.), and only rarely parts of lichens (Cladonia silvatica and Cetraria islandica). The adult individuals of C. quadridentata ate Pleurococcus sp. and Cladonia silvatica in equal frequency. The adult specimens of N. cf. coronata ate Pleurococcus sp. and raw potato. After several days females (C. quadridentata) started to deposit eggs. The hatched larvae and all nymphs ate only Pleurococcus sp. (N. coronata). The sum of effective temperatures for all three species was: Theoretical duration of development was calculated as (the results are given in Table 3): The present studies have shown that development of C. bipilis from the egg to the adult stage lasts on average 64-65 days at 17ºС and 43-44 days at 20ºС, development of C. quadridentata – 88-89 days at 17ºС and 57-58 days at 20ºС, and development of N. cf. coronata – 148-149 days at 20ºС and 112 days at 22.5ºС. Lower development threshold tempe- rature for all species is above 10ºС. The sum of effective temperatures, which are required for development of Ceratoppia species are 2-3 times lower than for N. cf. coronata. Length of development of Ceratoppia species and N. cf. coronata is given in Table 1. The comparison of development terms of N. cf. coronata nymphs is given in Table 2.

The duration of development in the examined species was different. At 20 ºС the development of Ceratoppia was much shorter than that of N. cf. coronata. This may be explained by the fact that mites from Brachypylina group (represented by C. bipilis and C. quadridentata) generally develop faster than those of early- derivative Macropylina (represented by N. cf. coronata) (Lebrun 1970, Norton & Palmer 1991). This finding is in contrast with earlier suggestions (Ghilarov 1982, Ryabinin & Pan΄kov 1987), that the generation time of parthenogenetic species is shorter than that of sexual species. Development within Ceratoppia species had dissimilarities as well. The duration of egg and nymphal stages of C. bipilis was shorter than in C. quadri- dentata, whereas durations of moults (periods of rest) were approximately identical. We noted that observed lengths of development in C. bipilis (53-73 days at 17ºС and 40-51 days at 20ºС) are comparable with those obtained by Krivolutsky (1995; 49-87 days at 18ºС, 79 days at room temperature).

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Table 1. (Continued) Table 2. The comparison of development time of N. cf. coronate nymphs at two temperatures (in days, PR: period of rest). The development time of N. cf. coronata at 22.5ºС (112 days) was similar to that of N. nana (Nicolet, 1855) examined by Sengbusch (1958). His experiments were carried out at 25°C and this species developed in 111 days. The most important difference between these two parthenogens was the duration time of eggs (N. cf. coronata proceeds twice as fast as N. nana). It is generally known, that temperature modifies the generation time of oribatid mites (Uvarov 2003, Ermilov 2004). Higher temperature affects respiration, trophic activity, reproduction and development favorably. In the present study we have shown that development of C. bipilis and C. quadridentata at 20°С is 1.5 times shorter than at 17°С, whereas development of N. cf. coronata at 22.5°С is about 1.3 times shorter than at 20°С. Table 3. The development duration of Ceratoppia bipilis, C. quadridentata and Nanhermannia cf. coronata (* calculated theoretically).

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Furthermore, each subsequent nymphal stage and its corresponding period of rest are longer than the previous. However, the reduction of temperature causes more considerable differences in duration between stages. The data support previous observations (Norton & Palmer 1991) that increase in temperature speeds up the development of oribatid mites, but do not support the prediction that a parthenogenetic species would have shorter generation time than the sexual species.

REFERENCES

Block, W. (1965): The life histories of Platynothrus peltifer (C.L. Koch, 1839) and Damaeus clavipes (Hermann, 1804) (Acarina: Cryptostigmata) in soils of Pennine Moorland. Acarologia 7: 735-743. Burn, A.J. (1986): Feeding rates of the cryptostigmatid mite Alaskozetes antarcticus. British Antarctic Survey Bulletin 71: 11–18. Chistyakov, M.P. (1970): Biology and postembrionic development Oppia nova (Oudem., 1902) (Oribatei) a dominating species of the developed turbaries of Gorkiy region. Uchenye zapiski Gorkovskogo pedagogicheskogo instituta. Gorkiy, GGPI 114: 51-64. Crossley, D.A. Jr. (1977): Oribatid mites and nutrient cycling, pp.71-85 in D.L. Dindal (editor). Biology of oribatid mites. State University of New York College of Environmental Science and Forestry, Syracuse. 122 pp. Ermilov, S.G. (ed.) (2004): Features of the population oribatid mites of large industrial centre (city of Nizhniy Novgorod). Nizhniy Novgorod 174 pp. Ermilov, S.G. (2006): The life cycle of oribatid mite Hydrozetes lemnae (Oribatei, Hydrozetidae). Zoologicheskiy zhurnal 85: 853-858. Ermilov, S.G., Chistyakov, M.P., Renzhina, A.A. (2004): The effect of temperature on the duration of development of Trhypochthonius tectorum (Berlese, 1896) (Acariformes, Oribatei). Povolzhskiy ecologicheskiy zhurnal 1: 87-90. Ermilov, S.G., Łochyńska, M., Olszanowski, Z. (2008): The cultivation and morphology of juvenile stages of two species from genus Scutovertex (Acari, Oribatida, Scutoverticidae). Annales Zoologici 58: 433-443. Ghilarov, M.S. (1982): The ecological value of parthenogenesis. Advances in Modern Biology (Moscow) 93: 10-22 (in Russian).. Hartenstein, R. (1962): Soil Oribatei. V. Investigation on Platynothrus peltifer (Acarina; Camisiidae). Annals of the Entomological Society of America 5: 709-713. Krivolutsky, D.A. (ed.) (1995): Oribatid mites: morphology, development, phylogeny, ecology, methods of study, the characteristic of modelling species Nothrus palustris C.L. Koch, 1839. Мoskva Nauka 224 pp. Lebrun, Ph. (1970): Écologie et biologie de Nothrus palustris (C.L. Koch, 1839). 3ème note: Cycle de vie. Acarologia 12: 193-207. Luxton, M. (1975): Studies of the oribatid mites of a Danish beech wood soil. II. Biomass, calorimetry and respirometry. Pedobiologia 15: 161-200. Luxton, M. (1981): Studies on the oribatid mites of a Danish beech wood soil. IV. Development biology. Pedobiologia 21: 312–340. MacArthur, R.H., Wilson, E.O. (1967): The theory of island biogeography. Princeton University Press, Princeton pp. 224. Maraun, M., Scheu, S. (2000): The structure of oribatid mite communities (Acari, Oribatida): patterns, mechanisms and implications for future research. Ecography 23: 374-382. Michael, A.D. (1884-1888): British Oribatidae. I-II. L.: Roy Soc. 657 pp. Nannelli, R. (1975): Osservazioni sulla biologia di Oppia concolor in condizioni sperimentali di allevamento. Redia 56: 11-116. Norton, R.A., Palmer, S.C. (1991): The distribution, mechanisms and evolutionary significance of parthenogenesis in oribatid mites. In: Schuster, R. and Murphy, P.W. (eds), The Acari: reproduction, development and life-history-strategies. Chapman and Hall, pp. 107-136.

Available online at www.ignited.in Page 6

Ryabinin, N.A., Pan΄kov, A.N. (1987): The role of parthenogenesis in biology of oribatid mites. Ecologia (Academia Nauka, USSR) 4: 62-64 (in Russian). Seniczak, S. (1972): A method of cultivation of mites in glass cultivation tubes with asbestous bottoms. Polish Journal of Soil Science 5: 127-132. Sengbusch, H.G. (1958): The development of Nanhermannia nana (Nicolet), (Acarina, Oribatei). Life history studies of Oribatei. II. Anat. Ree. V. 132. 3. pp. 504 Shaldybina, E.S. (1969а): The oribatid mites of superfamily Ceratozetoidea (their morphology, biology, systematization and a role in epizootic anoplocephalidose). Gorkiy 708 pp. Shaldybina, E.S. (1969b): The postembryonic development of Zetomimus furcatus (Pearce et Warb.), 1905 (Oribatei, Ceratozetoidea). Uchenye zapiski Gorkovskogo pedagogicheskogo instituta. Gorkiy, GGPI 99: 40-52. Siepel, H. (1994): Life-history tactics of soil microarthropods. Biology and Fertility of Soils 18: 263-278. Sitnikova L.G. (1959): Life cycles of some oribatid mites and their methods cultivation. Zoologicheskiy zhurnal 38: 1663-1673 (in Russian). Solhøy, T. (1975): Dynamics of Oribatei populations on Hardangervidda, pp. 111–116 in F. Wielgolaski (editor). Fennoscandian Tundra Ecosystems. Part 2: Animals and System Analysis. Springer-Verlag, Berlin. 337 pp. Subías, L.S. (2004) Listado sistematico, sinonimico y biogeografico de los acaros oribatidos (Acariformes: Oribatida) del mundo. Graellsia 60: 3-305. Uvarov, A.V. (2003): Effects of diurnal temperature fluctuations on population responses of forest floor mites. Pedobiologia 47: 331-339. Webb, N.R. (1977): Observations on Steganacarus magnus. General biology and life cycle. Acarologia 19: 686-696. Weigmann, G. (1975): Labor- und Freilandunster- suchungen zur Generationsdauers von Oribatiden (Acari: Oribatei). Pedobiologia 15: 133-148.