Nosema bombi: A pollinator parasite with detrimental fitness effects Oliver Otti a, * , Paul Schmid-Hempel a,b a Experimental Ecology, Institute of Integrative Biology Zurich (IBZ), ETH Zurich, 8092 Zurich, Switzerland b Wissenschaftskolleg zu Berlin, Wallotstrasse 19, D-14193 Berlin, Germany Received 30 October 2006; accepted 27 March 2007 Available online 31 March 2007 Abstract Nosema bombi is an obligate intracellular parasite that infects different bumblebee species at a substantial, though variable, rate. To date its pathology and impact on host fitness are not well understood. We performed a laboratory experiment investigating the pathology and fitness effects of this parasite on the bumblebee Bombus terrestris. We experimentally infected one group of colonies with N. bombi spores at the start of the worker production, while a second uninfected group of colonies served as controls. During colony development we collected live workers for dissections to measure infection intensities. In parallel, we measured several life history traits, to investigate costs to the host. We succeeded in infecting 11 of 16 experimental colonies. When infection occurred at an early stage of colony devel- opment, virtually all individuals were infected, with spores being found in a number of tissues, and the functional fitness of males and young queens was reduced to zero. Further, the survival of workers from infected colonies and infected males were reduced. With such severe effects, N. bombi appears to decrease its opportunities for transmission to the next host generation. Ó 2007 Elsevier Inc. All rights reserved. Keywords: Host–parasite interaction; Nosema bombi; Bombus terrestris; Pathology; Fitness effects; Microsporidia; Virulence; Pollinator parasites 1. Introduction Bumblebees are important natural pollinators for a wide range of flowering plants (Goulson, 2003) and are of eco- nomic importance as they pollinate a substantial propor- tion of our crops. They are therefore commercially bred in large numbers to be used in the pollination of a range of greenhouse crops, such as tomato, capsicum and melon (Al-Attal et al., 2003; Banda and Paxton, 1991; de Ruijter, 1997). In the United States alone, the annual economic value of pollination services is estimated at 1.25 billion USD, of which bumblebees provide a large share (Ghazoul, 2005). These major ecological and economic roles have led to widespread concern over recent declines in pollinator populations, including bumblebees (Goulson, 2003; Wil- liams, 2003). The major causes of this decline are thought to relate to changes in the use of agricultural land (Goulson et al., 2005; Williams, 2005), but also the effects of parasites could play a role in reducing populations, at least when they invade populations that are diminishing for other reasons. Studies on other economically important insect species, e.g. the silkworm moth and the honeybee, have shown that parasites can inflict substantial financial losses to managed populations. For example, in the 19th century, the micro- sporidian parasite N. bombycis, the agent of pebrine disease in the silkworm Bombyx mori (an insect important for the production of textiles), was spread throughout France and caused massive losses to the silk industry (Cadeddu, 2000). Currently, the Varroa mite in honeybees poses financial problems to the apiculture industry as it impairs the honey production and kills off reproductive animals so that the colonies can no longer be propagated (Sammataro et al., 2000). In the United States, the industry is under additional pressure due to the spread of the Africanized honeybee (Whitfield et al., 2006). There is, however, a concern that a parasite, the microsporidian Nosema bombi Fantham and Porter, 1914, could cause the decline of the native bumblebee community (Kearns and Thomson, 2001; Whit- tington and Winston, 2003), but too little is known to date 0022-2011/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jip.2007.03.016 * Corresponding author. Fax: +41 44 632 1271. E-mail address: oliver.otti@env.ethz.ch (O. Otti). www.elsevier.com/locate/yjipa Journal of Invertebrate Pathology 96 (2007) 118–124 Journal of INVERTEBRATE PATHOLOGY