The thermal environment of the nest affects body and cell size in the solitary red mason bee (Osmia bicornis L.)

Highlights

• Bees developing in semi-natural nests of various thermal conditions were studied.

• In warmer temperature bees developed lower body mass and smaller ommatidia.

• Both mean and variance of temperature affected body and cell size of bees.

• Male bees tended to have larger ommatidia than females of the same body mass.

Abstract

Many ectotherms grow larger at lower temperatures than at higher temperatures. This pattern, known as the temperature-size rule, is often accompanied by plastic changes in cell size, which can mechanistically explain the thermal dependence of body size. However, the theory predicts that thermal plasticity in cell size has adaptive value for ectotherms because there are different optimal cell-membrane-to-cell-volume ratios at different temperatures. At high temperatures, the demand for oxygen is high; therefore, a large membrane surface of small cells is beneficial because it allows high rates of oxygen transport into the cell. The metabolic costs of maintaining membranes become more important at low temperatures than at high temperatures, which favours large cells. In a field experiment, we manipulated the thermal conditions inside nests of the red mason bee, a solitary bee that does not regulate the temperature in its nests and whose larvae develop under ambient conditions. We assessed the effect of temperature on body mass and ommatidia size (our proxy of cell size). The body and cell sizes decreased in response to a higher mean temperature and greater temperature fluctuations. This finding is in accordance with predictions of the temperature-size rule and optimal cell size theory and suggests that both the mean temperature and the magnitude of temperature fluctuations are important for determining body and cell sizes. Additionally, we observed that males of the red mason bee tend to have larger ommatidia in relation to their body mass than females, which might play an important role during mating flight.

Introduction

In 1847, Carl Bergmann reported that the body size of endotherms is positively correlated with geographic latitude. Bergmann proposed the role of increased heat conservation capacity in larger animals associated with their relatively small body surface area as an adaptive mechanism (Voorhies, 1996). Similar latitudinal clines in body size were recently discovered in ectotherms, indicating that the heat-conservation hypothesis cannot be universally applied to all types of organisms. Moreover, many ectotherms respond plastically to thermal developmental conditions by emerging at larger adult sizes in colder conditions than in warmer ones, in a pattern called the temperature-size rule (Atkinson, 1994). Limited evidence suggests that ectotherms respond to different developmental temperatures by changing not only body size but also cell size (Blanckenhorn and Llaurens, 2005, De Moed et al., 1997, French et al., 1998; Van Voorhies, 1996). According to the theory of optimal cell size (TOCS), the thermal sensitivity of cell size has fitness consequences (Atkinson et al., 2006, Czarnoleski et al., 2013, Czarnoleski et al., 2015, Kozłowski et al., 2003, Szarski, 1983). Czarnoleski et al. (2013) argued that because oxygen permeates more readily through lipids in membranes than through the aqueous environment in the cytosol (Subczynski et al., 1989), a tissue built of small cells provides a more extensive network of cellular membranes for oxygen distribution than does a tissue built of large cells. Consistent with this interpretation, fruit flies develop small cells under poor oxygen conditions (Heinrich et al., 2011, Zhou et al., 2007). Similarly, a high demand for oxygen in warm environments favours small cells, which increase the rate of oxygen delivery to mitochondria, even under normoxia. However, a tissue that consists of numerous small cells should be more costly than one consisting of fewer, large cells because a large part of the cellular energetic budget is devoted to the maintenance of the physiological functionality of cell membranes (Kozłowski et al., 2003). According to Czarnoleski et al. (2013), the low demand for oxygen in cold environments does not justify costly small cells.

Experiments on the thermal sensitivity of cells and body size have been typically performed under controlled laboratory conditions (e.g., Czarnoleski et al., 2013, Czarnoleski et al., 2015; Partridge et al., 1994), and complementary evidence from thermal experiments set in semi-natural conditions is lacking. Here, we performed a field experiment with the solitary red mason bee (Osmia bicornis, Linnaeus) to assess the role of the thermal environment inside nests in influencing cell size and body size among emerging bees. In contrast to social bees such as the honeybee (Bonoan et al., 2014) and bumblebees (O’Donnell and Foster, 2001, Weidenmüller et al., 2002), solitary bees do not regulate the temperature inside their nests. Because access to nesting sites is limited (Potts et al., 2005, Steffan-Dewenter and Schiele, 2008), solitary bees appear to typically develop over a wide range of thermal conditions, suggesting that experiencing thermal variations is a part of their biology. We manipulated the thermal environment of developing larvae by restricting female establishment of nests to the following three types of sites: two naturally occurring microhabitats, one constantly exposed to full sun (sun site) and one shaded (shade site); and a warm and temperature-constant environment, which was artificially created by heating the nests to the desired temperature (heated site). Using this design, we created a range of thermal conditions, with site differences in mean temperature (sun and heated vs. shade) and thermal variance (heated vs. sun). Based on the temperature-size rule and the TOCS, we expected that warm nests and thermally fluctuating nests would result in smaller bees that consisted of smaller cells.