Sex-specific volatile compounds influence microarthropod-mediated fertilization of moss

Abstract

Sexual reproduction in non-vascular plants requires unicellular free-motile sperm to travel from male to female reproductive structures across the terrestrial landscape. Recent data suggest that microarthropods can disperse sperm in mosses. However, little is known about the chemical communication, if any, that is involved in this interaction or the relative importance of microarthropod dispersal compared to abiotic dispersal agents in mosses. Here we show that tissues of the cosmopolitan moss Ceratodon purpureus emit complex volatile scents, similar in chemical diversity to those described in pollination mutualisms between flowering plants and insects, that the chemical composition of C. purpureus volatiles are sex-specific, and that moss-dwelling microarthropods are differentially attracted to these sex-specific moss volatile cues. Furthermore, using experimental microcosms, we show that microarthropods significantly increase moss fertilization rates, even in the presence of water spray, highlighting the important role of microarthropod dispersal in contributing to moss mating success. Taken together, our results indicate the presence of a scent-based 'plant-pollinator-like' relationship that has evolved between two of Earth's most ancient terrestrial lineages, mosses and microarthropods.

Passive warming reduces stress and shifts reproductive effort in the Antarctic moss,Polytrichastrum alpinum

“…Recent work found that warming reduced Collembollan populations in an Antarctic lichen community (Bokhorst et al, 2015). If mosses increase reproductive efforts in response to warming by producing more gametangia, but the resident microarthropods who assist in sperm dispersal (see Rosenstiel et al, 2012) are differentially sensitive to warming, this evolving scenario could present a new barrier to reproduction in dioicous mosses of Antarctica. Evidence of the negative impacts of climate change among species due to phenology shifts are becoming common in the literature (e.g.…”

“…Previous work demonstrates the important role of microarthropods (mostly Collembolans) in increasing moss sexual reproduction through mediating sperm dispersal (Cronberg et al, 2006;Cronberg, 2012;Rosenstiel et al, 2012), and perhaps an active microarthropod community is another necessary ecological requirement for sexual reproduction in Antarctic dioicous species. Studies examining the impacts of simulated warming on plant-dwelling microarthropods in the WAP found that although ubiquitous in both mesic and extreme environments, Collembolans were particularly sensitive to changes in temperature and moisture Day et al, 2009).…”

“…However, recent studies showed that dioicous mosses are more genetically diverse than would be expected with such dispersal limitation (Wyatt et al, 1989;Van der Velde et al, 2001;Wilson and Provan, 2003). Indeed several studies have since demonstrated greater sperm dispersal distances (for a review, see Glime, 2007), as well as stresstolerant sperm (Rosenstiel and Eppley, 2009;Shortlidge et al, 2012) and microarthropod-mediated sexual reproduction (Cronberg et al, 2006;Cronberg, 2012;Rosenstiel et al, 2012). Other factors can limit sexual reproduction in mosses, including: inadequate resources (Stark et al, 2000) growth trade-offs (Ehrlén et al, 2000) and investment in environmental stress defence (Convey and Smith, 1993;Stark et al, 2009;Eppley et al, 2011).…”

Mites on Plants

“…Species in the families Achipteriidae, Ameronothridae, Camisiidae, Carabodidae, Ceratozetidae, Crotoniidae, Damaeidae, Eremaeidae, Galumnidae, Hammeriellidae, Liacaridae, Liodidae, Megeremaeidae, Micreremidae, Mochlozetidae, Mycobatidae, Nanhermanniidae, Oppiidae, Oribatulidae, Oripodidae, Pedrocortesellidae, Peloppiidae, Phenopelopidae, Phthiracaridae, Tectocepheidae and Xenillidae all are commonly found associated with moss and other 'cryptogams' on tree trunks and branches (Walter and Behan-Pelletier 1999 ). In spite of this association and strong evidence that oribatid mites and other microarthropods have a 'pollinator-like' relationship with mosses (Cronberg et al 2006 ;Rosenstiel et al 2012 ), there is little indication that oribatid mites feed on moss leaves. However, in the eucalyptus forests of north Queensland, Birobates hepaticolus (Oripodidae), both lives in and feeds on a bark-inhabiting leafy liverwort (Colloff and Cairns 2011 ).…”

Mass-occurrence of springtails onTortula cernua(Huebener) Lindb.: a field-observation of possible animal-mediated fertilization

“…We therefore asked whether our discovery might represent an example of springtail-mediated fertilization, akin to that recently shown in experimental settings by Cronberg et al (2006) and Rosenstiel et al (2012). In the laboratory, we carefully examined the portion of the collection (ca 2|3 cm) where springtails were most abundant.…”