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Altitudinal variation in size and composition of eggs in the land snail Arianta arbustorum A. Baur and B. Baur

Abstract: Egg size and egg provisioning are crucial for the survival of offspring in invertebrates without postlaying egg care. The effects of elevation and size of the mother on egg size and on nitrogen and carbon concentrations in eggs were examined in eight populations of the land snail Arianta arbustorum over an altitudinal gradient from 370 to 2340 m in Switzerland. The dry mass of single eggs ranged from 1.48 to 2.79 mg and decreased with increasing altitude. Adult snail size (shell volume) also decreased with increasing elevation as did clutch size and reproductive investment (clutch size × egg dry mass) of mothers. Hatching success of eggs varied among populations, but showed no altitudinal pattern. When differences in parental shell size were taken into account, correlations between altitude and egg size, clutch size, and reproductive investment disappeared. Thus, the altitudinal decreases in egg size, clutch size, and reproductive investment were mainly due to smaller snail sizes at higher elevations. The nitrogen concentration in eggs ranged from 3.4 to 4.5% and decreased with increasing elevation. In contrast to egg and clutch size, the altitudinal variation in nitrogen concentration of eggs cannot be explained by differences in snail size. The carbon concentration in eggs ranged from 31.1 to 33.1%, but showed no altitudinal variation. Nitrogen and carbon concentrations in the eggshell and egg fluid in eggs from four populations were examined separately. The nitrogen concentration in the eggshell ranged from 0.7 to 1.8% and was lower than that of the egg fluid (5.1–5.8%). Similarly, the carbon concentration in the eggshell was lower (20.2–22.8%) than that in the egg fluid (35.8−40.2%). Interpopulation differences in egg composition may affect growth, size, and survival of hatchlings and the extent of egg cannibalism in A. arbustorum. Résumé : La taille des oeufs et leur approvisionnement sont des facteurs critiques pour la survie de la progéniture chez les invertébrés qui n’apportent pas de soins postnataux à leurs oeufs. Les effets de l’altitude et de la taille de la mère sur la taille des oeufs et sur les concentrations d’azote et de carbone dans les oeufs ont été examinés chez huit populations de l’escargot Arianta arbustorum le long d’un gradient altitudinal de 370 à 2 340 m en Suisse. La masse sèche d’un oeuf allait de 1,48 à 2,79 mg et diminuait à mesure que l’altitude augmentait. La taille des escargots adultes (volume de la coquille) diminuait aussi en fonction inverse de l’altitude, comme d’ailleurs la taille des couvées et l’investissement reproducteur (taille de la couvée × masse sèche d’un oeuf) des mères. Le succès à l’éclosion variait selon la population, mais n’était pas relié à l’altitude. Lorsque les différences de taille des coquilles chez les parents sont prises en compte, les corrélations entre l’altitude et la taille des oeufs, la taille des couvées et l’investissement reproducteur disparaissent. Les diminutions de la taille des oeufs, de la taille des couvées et de l’investissement reproducteur en fonction de l’altitude sont donc dues surtout à la taille plus petite des gastropodes aux altitudes plus élevées. La concentration d’azote des oeufs se situait entre 3,4 et 4,5% et diminuait en altitude. Contrairement à la taille des oeufs et à la taille des couvées, la variation altitudinale de la concentration d’azote dans les oeufs ne peut s’expliquer par des différences de taille entre les escargots. La concentration de carbone des oeufs se situait entre 31,1 et 33,1%, mais ne variait pas avec l’altitude. Les concentrations d’azote et de carbone dans la coquille et dans le fluide des oeufs ont été examinées séparément chez quatre populations d’escargots. La concentration d’azote se situait entre 0,7 et 1,8%, concentration inférieure à celle rencontrée dans la partie fluide des oeufs (5,1–5,8%). De même la concentration de carbone de la coquille était plus faible (20,2–22,8%) que celle du fluide des oeufs (35,8–40,2%). Chez A. arbustorum, les différences de composition des oeufs d’une population à l’autre peuvent affecter la croissance, la taille et la survie des gastropodes fraîchement éclos et l’importance du cannibalisme exercé sur les oeufs. [Traduit par la Rédaction]

Baur and Baur

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The size of eggs and their energy and nutrient contents are important determinants of offspring survival in animals without postlaying egg care (Clutton-Brock 1991). Egg size is Received January 12, 1998. Accepted June 11, 1998. A. Baur1 and B. Baur. Department of Integrative Biology, Section of Conservation Biology (NLU), University of Basel, St. Johanns-Vorstadt 10, CH-4056 Basel, Switzerland. 1

Author to whom all correspondence should be addressed (e-mail: [email protected]).

Can. J. Zool. 76: 2067–2074 (1998)

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commonly related to the survival, growth, and eventual breeding success of offspring, although this is not always the case (Karlsson and Wicklund 1984; Stearns 1992). In an evolutionary context, two different solutions to the problem of increasing maternal nutrition can be recognized in gastropods: increasing egg size and producing nurse eggs (Baur 1992). The probability of survival of newly hatched gastropods is likely to increase with hatchling size, which in turn is positively related to egg size except in the case of nurse-egg feeders (Spight et al. 1974; Spight 1976a, 1976b). The production of nurse eggs is restricted to marine prosobranch gastropods (Fioroni 1988). In terrestrial gastropods, provisioning © 1998 NRC Canada

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Can. J. Zool. Vol. 76, 1998 Table 1. Description of localities in Switzerland from which adult A. arbustorum were obtained. Locality

Altitude (m asl)

Aesch

370

Arlesheim

380

Étang d’Oye

830

Mont Raimeux

1290

Gurnigel

1430

Gantrisch Strela

1800 2180

Schiawang

2340

Habitat description

N

Grass-covered clearing in a coniferous forest, 10 km S of Basel (47°28′N, 7°34′E) Grass-covered embankment of a pond, 7 km SE of Basel (47°30 ′N, 7°38′E) Verge of a track covered with rough herbage and bushes, 47 km SW of Basel (47°17′N, 7°06 ′E) Pasture interspersed with trees on the north-facing slope of Mont Raimeux, 30 km SW of Basel (47°18′N, 7°26 ′E) Embankment of a track in a coniferous forest, 20 km S of Bern (46°44′N, 7°27′E) Alpine pasture, 25 km S of Bern (46°42 ′N, 7°27′E) Alpine pasture with scattered scree on a NW-facing slope, 4 km W of Davos (46°49′N, 9°48′E) Alpine pasture on a south-facing slope, 3 km W of Davos (46°49′N, 9°49′E)

9 13 12 10 13 12 12 12

Note: N is the number of snails collected.

of eggs with energy, nutrients, and calcium carbonate is the most common form of parental investment (Baur 1994a). The structure and composition of eggs have been analyzed in a variety of land snail species (reviewed by Bayne 1968; Tompa 1984). In general, eggs of terrestrial gastropods are rich in proteins, mucopolysaccharides, and calcium carbonate (Duncan 1975; Tompa 1984). For example, the protein concentration in freshly laid eggs averaged 38.8% of their dry mass in Sphincterochila boissieri and 25.6% in Arianta arbustorum (Yom-Tov 1971; Baur 1994). However, intraspecific variation in egg composition has not been examined in terrestrial gastropods, except in A. arbustorum (Baur 1994; Baur and Baur 1997). Previous studies showed that the variation in nitrogen and carbon concentrations in eggs within single batches was smaller than the corresponding variation in egg size (Baur 1994). Eggs of successive batches showed seasonal variation in nitrogen and carbon concentrations (Baur and Baur 1997). Egg size and nutrient concentration may vary in different environments as a result of different selection pressures (e.g., Goulden et al. 1987). On mountain slopes the climate becomes more adverse and daily temperature fluctuations are more pronounced with increasing elevation (Franz 1979). Furthermore, at high altitudes, the time available for reproduction is reduced to a few weeks, which affects the life history of A. arbustorum (Baur and Raboud 1988). In the present study we examined intraspecific variation in size and composition of eggs in eight A. arbustorum populations in Switzerland over an altitudinal gradient ranging from 370 to 2340 m. The analyses were directed to answering three main questions: (1) do eggs from different A. arbustorum populations differ in size, nitrogen, and carbon concentrations, (2) are size and composition of eggs affected by the size of the mother, and (3) do possible interpopulational differences in egg size and egg composition correlate with the altitude of the population?

Study animal Arianta arbustorum is a simultaneously hermaphroditic land snail common in moist habitats of northwestern and central Europe

(Kerney and Cameron 1979; Baur 1986). The snail has determinate growth; individuals become sexually mature at 2 − 4 years of age and live for a further 3− 4 years (maximum 14 years; Baur and Raboud 1988). Adult snails measure 16 − 20 mm in shell diameter. In the field, snails deposit one to three batches, each consisting of 20–80 eggs, per reproductive season. The eggs are laid in small holes in the soil or in decaying grass or moss (Baur 1988a). The nearly spherical eggs are approximately 3 mm in diameter (Baur 1984). Eggshells of A. arbustorum are partly calcified, with discrete crystals of calcium carbonate in a jelly matrix (cf. Bayne 1968). Hatching takes place 2 − 4 weeks after oviposition, depending on temperature. After emergence, hatchlings of A. arbustorum devour the remains of their eggshell and consume unhatched sibling eggs, including those with fully developed embryos (Baur and Baur 1986; Baur 1992).

General methods Eggs were obtained from adult A. arbustorum that were collected at eight localities (referred to, for convenience, as populations) situated at different altitudes in the lowlands, Jura Mountains, and Alps in Switzerland (Table 1). Nine to 13 adult individuals were collected from each population at the beginning of the reproductive season in 1993 and transported to the laboratory. The snails were kept singly in transparent beakers (8 cm deep, 6.5 cm in diameter) with moist soil (approximately 3 cm deep) in the bottom at 19°C and on a cycle of 18 h light : 6 h dark. The beakers were cleaned and checked for eggs twice per week, and fresh lettuce was provided ad libitum as food. Lettuce contains all necessary nutrients in sufficient amounts for egg production (Baur 1994). The eggs of each batch were collected, cleaned on a moist paper towel, counted, and kept separately in a plastic dish (6.5 cm in diameter) lined with moist paper towelling for at least 24 h (maximum 3 days) before further treatment. Newly laid eggs of A. arbustorum absorb water from the environment to reach their normal turgid state. The diameters of eight randomly chosen eggs from each batch were measured to the nearest 0.04 mm using a binocular microscope with a stage micrometer. These eggs were then dried for 72 h at 70°C 10–14 days before their nutrient content was analyzed. The nitrogen and carbon concentrations of single eggs were determined using a CHN analyzer (LECO CHN-900, LECO Instruments GmbH, Munich, Germany). The dry mass of each egg was recorded to the nearest 0.01 mg using a balance connected to the CHN analyzer. Reproductive investment was defined as clutch size × egg dry mass (in milligrams). In all, 1200 single eggs from 150 batches and 93 parental snails were analyzed. The remaining eggs of each clutch were kept at 19°C to determine hatching suc© 1998 NRC Canada

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Table 2. Differences in maternal size and egg parameters in eight A. arbustorum populations. Population (altitude; m asl)

Mother’s size (shell volume; cm3)

Egg volume (mm3)

Egg dry mass (mg)

Clutch size (no. of eggs)

Hatching success (%)

Aesch (370) Arlesheim (380) Étang d’Oye (830) Mont Raimeux (1290) Gurnigel (1430) Gantrisch (1800) Strela (2180) Schiawang (2340)

2.27±0.12 2.97±0.10 1.97±0.09 1.42±0.04 1.27±0.04 1.27±0.04 1.28±0.05 0.73±0.04

13.13±0.49 14.93±0.49 12.65±0.28 10.91±0.48 11.83±0.31 11.33±0.50 11.87±0.34 10.05±0.32

2.26±0.06 2.79±0.06 2.22±0.06 2.41±0.09 2.14±0.03 2.03±0.07 1.84±0.06 1.48±0.05

81.5±5.2 56.2±4.2 66.0±4.3 55.1±4.9 34.5±1.6 26.5±1.9 38.0±2.8 23.3±2.8

83.4±4.4 (13)a 85.9±3.2 (25)ab 51.1±11.3 (12)b 68.1±6.6 (13)ab 80.5±4.0 (33)ab 80.9±6.3 (12)ab 72.4±6.2 (30)ab 74.7±6.6 (12)ab

F P

109.99