A test for Allee effects in the self-incompatible
wasp-pollinated milkweed Gomphocarpus physocarpus
GARETH COOMBS,
1
CRAIG I. PETER
1
* AND STEVEN D. JOHNSON
2
1
Department of Botany, Rhodes University, PO Box 94, Grahamstown, 6140, South Africa (Email:
c.peter@ru.ac.za), and
2
Centre for Invasion Biology, School of Conservation and Biological Sciences,
University of KwaZulu-Natal, Scottsville, South Africa
Abstract It has been suggested that plants that are good colonizers will generally have either an ability to
self-fertilize or a generalist pollination system. This prediction is based on the idea that these reproductive traits
should confer resistance to Allee effects in founder populations and was tested using Gomphocarpus physocarpus
(Asclepiadoideae: Apocynaceae), a species native to South Africa that is invasive in other parts of the world.We
found no significant relationships between the size of G. physocarpus populations and various measures of pollina-
tion success (pollen deposition, pollen removal and pollen transfer efficiency) and fruit set. A breeding system
experiment showed that plants in a South African population are genetically self-incompatible and thus obligate
outcrossers. Outcrossing is further enhanced by mechanical reconfiguration of removed pollinaria before the
pollinia can be deposited. Self-pollination is reduced when such reconfiguration exceeds the average duration of
pollinator visits to a plant. Observations suggest that a wide variety of wasp species in the genera Belonogaster and
Polistes (Vespidae) are the primary pollinators.We conclude that efficient pollination of plants in small founding
populations, resulting from their generalist wasp-pollination system, contributes in part to the colonizing success of
G. physocarpus. The presence of similar wasps in other parts of the world has evidently facilitated the expansion of
the range of this milkweed.
Key words: Allee effect, Asclepiadoideae, Gomphocarpus physocarpus, pollen transfer efficiency, pollinarium recon-
figuration, self-incompatible, wasp pollination.
INTRODUCTION
The fitness of individuals is frequently positively
related to either the number or density of conspecifics
(Allee 1931). This phenomenon has become known
as the Allee effect (Groom 1998; Courchamp et al.
1999; Stephens & Sutherland 1999; Stephens et al.
1999). The basis for Allee effects may be genetic
(Charlesworth & Charlesworth 1987; Ellstrand &
Elam 1993; Courchamp et al. 1999; Herlihy & Eckert
2002) or ecological, as in reduced cooperative inter-
actions between individuals in small or sparse popu-
lations (Groom 1998; Courchamp et al. 1999). There
may also be interactions between ecological and
genetic effects. For example, small plant populations
may be less attractive to foraging insect pollinators
because of reduced floral display and rewards
(Schmidt-Hempel & Speiser 1988; Klinkhamer & de
Jong 1990; Goulson 1999; Thompson 2001). Pollina-
tors that do visit small populations may, in turn, also
increase their intrapatch foraging time culminating in
increased self-pollination, which in self-compatible
plants leads to inbreeding (de Jong et al. 1993;
Oostermeijer 2003). Self-pollination can also com-
promise the export of pollen by wasting pollen that
potentially could have been exported. This process is
known as pollen discounting (de Jong et al. 1993).
Most attention has been paid to Allee effects in rare
native species (Ward & Johnson 2005).The persistence
of small populations is, however, undoubtedly also
important for colonizing and invasive species (Lieb-
hold & Bascompte 2003; Taylor & Hastings 2005; Van
Kleunen & Johnson 2005). Single founders, in particu-
lar, would be more likely to establish populations
if they are able to self-fertilize (Baker 1955), as they
would be relatively immune from ecological Allee
effects because of an absence of pollinators or mates.
Available data suggest that there is a tendency for Allee
effects to be weakened or absent in self-compatible
plant species (Leimu et al. 2006).
Several studies have demonstrated that plants in
small populations often show markedly increased seed
production following supplemental hand-pollinations
using pollen from within the same population (Ågren
1996; Ward & Johnson 2005). This provides direct
evidence for ecological Allee effects through decreased
pollinator visitation in small populations. On the other
hand, pollination success is seemingly unaffected by
population size in other plant species (Kunin 1993,
*Corresponding author.
Accepted for publication October 2008.
Austral Ecology (2009) 34, 688–697
© 2009 The Authors doi:10.1111/j.1442-9993.2009.01976.x
Journal compilation © 2009 Ecological Society of Australia