POLLINATION OF POLISH RED LIST PLANTS : A PRELIMINARY STATISTICAL SURVEY

One of the important problems of modern conservation biology is the lack of reliable data on plant pollination systems, especially for taxa threatened with extinction. This paper is an attempt to collect and analyze the available literature data on pollination of Polish red list plants. The Polish red list includes 469 angiosperm taxa, over 53% of them are insect-pollinated and visited mostly by bees and fl ies, insects that are also declining in Europe. These numbers however are mainly based on lists of fl ower visitors and detailed studies of pollination biology or breeding system are available for less than 20% of the taxa, with further 10% almost completely unstudied in terms of their life histories. The paper indicates that there is an urgent need to study plant-pollinator relationships in order to better conserve the biodiversity in local and global scales.


INTRODUCTION
We are increasingly aware that conserving biodiversity means not only conserving particular taxa but conserving the healthy functioning of all parts of world ecosystems, including various interactions among living organisms, e.g.pollination (B u c h m a n n and N a b h a n , 1996; K e a r n s et al. 1998; T h o m p s o n , 2002; W a s e r and M a y f i e l d , 2006).
Although human understanding and interest in pollination of some plant species may be traced back to ancient times (P r o c t o r et al. 1996; C r e s t i and L i n s k e n s , 1999), the knowledge of the actual mechanisms of pollination biology and ecology is a relatively recent achievement of human science (W a s e r and M a y f i e l d , 2006).In spite of the explosive development of pollination studies in the last several decades (Fig. 1), there are few plant groups and species which have been thoroughly surveyed, with still a lot of anecdotic information on numerous plants that obscures rather than shows the actual 'state of the art'.This is especially important in case of endangered taxa.If we consider that losing all pollinators may, at the worst, mean losing 90% of fl owering plant species (W a s e r and M a y f i e l d , 2006), the knowledge of plant breeding systems seems one of essential issues in all conservation endeavors involving fl owering plants.Unfortunately, our lack of information on the biology and ecology of many plants as well as on the nature of relationships with animal pollinators may cause that even carefully design restoration projects are likely to fail if regeneration of endangered plant populations ceases.This for instance may be due to insect shortage as there is increasing evidence of the decline of pollinators (B u c h m a n n and N a b h a n , 1996; A l l e n -W a r d e l l et al. 1998; K e a r n s et al. 1998; B i e s m e i j e r et al. 2006;Va m o s i et al. 2006).
Recently there have been several attempts to estimate world (e.g.K l e i n et al. 2007) and Polish crop plants' (Z y c h and J a k u b i e c , 2006) dependence on animal pollinators but the evidence for endangered plant taxa is scarce.To our knowledge, there is no such statistics for the Polish fl ora, therefore, based on available literature, we attempted to analyze pollination systems of Polish red list plants with the emphasis on key pollinator agents.

MATERIALS AND METHODS
The Polish fl ora is composed of approx.2400 vascular plant species (M i r e k et al. 2002).The recently published Red list of the vascular plants in Poland includes approx.20% species of the Polish fl ora assigned to seven categories: extinct (Ex), extinct in the wild (EW), declining -critically endangered (E), vulnerable (V) and rare (R) (Z a r z y c k i and S z e l ą g , 2006; authors do not translate the categories according to IUCN standards).We extracted information on pollination of these plants from the available literature and from our own studies.We were especially interested in the nature of pollination systems of Polish red list plants (anemogamy, hydrogamy, zoogamy or autogamy; for simplicity, we treated autogamous and asexual, e.g.apomictic, taxa together and included in this category only obligate autogams, excluding facultatively autogamous plants), and key pollinators.As the length of this paper is limited, the list of the species with the references of the case studies for particular taxa is not included in the text and may be obtained from the authors upon individual request.

RESULTS
The Polish red list comprises 469 angiosperm taxa: 40 of them are extinct, 1 extinct in the wild, 140 endangered, 182 vulnerable and 106 rare and potentially endangered.The prevailing part of this group, over 53% (249 taxa), is insect-pollinated (entomogamous).From the remaining plants, 122 taxa are anemogamous (26%), seven are hydrogamous (1.5%), and 41 obligatory autogamous or asexual (9%).Three species exhibit mixed pollination systems: two of them (Helianthemum rupifragium and Salix lapponum) are ambophilous (windand insect-pollinated) and one (Hydrilla verticillata, Hydrocharitaceae) is reported as hydro-and anemogamous.For over 10% of the Red list plants (47 taxa), the literature data on pollination is defi cient or at least it was unavailable for the authors of the present study (Tab.1).
The most important pollinating agents of the entomogamous taxa are hymenopterans (mainly wild bees and honey bee); they are responsible (at least partly) for pollinations of over 73% of these plants.(numbers do not add to 100% as some plants may be pollinated and/or visited by several orders of insects, Fig. 2).
The available literature contains very scarce information on plant breeding systems.We were only able to fi nd data on this aspect of plant biology for approx.12% of the surveyed plants, 44 of them are reported to be self-compatible and 13 self-incompatible.

DISCUSSION
Numerous plant taxa become endangered and face extinction mainly due to habitat loss, their populations become fragmented and increasingly smaller.In some cases, this trend may be reversed by successful restorations.It is however limited by several environmental and biological factors.For zoogamous plants, one of the reasons of unsuccessful restorations may be the pollination failure that may restrain natural regeneration of endangered plant populations (K w a k and B e k k e r , 2006).This may be due to pollinator shortage and/or the specialized nature of plant-pollinator relationships (W i l c o c k and N e i l a n d , 2002).The results of the present survey show that at least 54% of the Polish Red list plants are entomogamous or ambophilous, which means that, at least partially, in their reproduction they are dependent on insect pollinators.Confronting this result with the growing evidence that also pollination systems are under increasing threat from anthropogenic sources, including habitat fragmentation, changes in land use, modern agricultural practices, pesticides and herbicides (A l l e n -W a r d e l l et al. 1998; K e a r n s et al. 1998; K r e m e n and R i c k e t t s ; 2000, K w a k and B e k k e r , 2006), shows the range of the problem to be faced by conservation biologists.
Most of the entomogamous Polish red list plants are pollinated by bees and fl ies (Fig. 2).A situation similar to this is found e.g. in the Netherlands (K w a k and B e k k e r , 2006), and the same groups, with bees being the most vulnerable, are also the most threatened in Europe.As reported by Biesmeijer et al. (2006) there were statistically signifi cant declines in bee diversity in 52% of UK's and 67% of the Netheralnds' 100 km 2 cells which were used by the authors for assessing the pollinator diversity in these two countries.Hoverfl ies' populations also surveyed in this study seem to be in slightly better conditions (decline in 33% vs. increase in 25% of the British cells, and increase in 34% and decline in 17% cells of the Dutch cells).This, however, does not compensate for the loss of wild bees.Even in cases where the given plant is pollinated by one key agent, there may be a net gain in resulting seed production form the interactions of various pollinator groups (W es t e r k a m p and G o t t s b e r g e r , 2000; K l e i n et al. 2003; G r e e n l e a f and K r e m e n , 2006); the diversity of the plant-pollinator interactions enhances also the persistence of plant communities (F o n t a i n e et al. 2006).Studies from Europe and other continents suggest that there is a causal relationship between the pollinator and fl owering plant decline (B i e s m e i j e r et al. 2006; Va m o s i et al. 2006).The species that are most likely to go extinct fi rst are those with the smallest populations and the most dispersed distribution.
When compared to the western Europe, the situation in Poland seems more stable due to higher diversity of agricultural landscapes still present in the country, but still there is an observed decrease in diversity and density of wild bees associated e.g. with xerothermic grassland communities (B a n a s z a k , 1992, 1997; B a n a s z a k et al. 2003), and a decline in bumblebee abundance is observed in many regions of the country (K o s i o r , 1995; R u s z k o w s k i and B i l i ń s k i , 1995).
Apart from the importance of insect pollinators to the preservation of endangered plant taxa, the present study shows also gaps in our knowledge.First, over 10% of the Red list plants (Tab. 1) are completely unstudied in terms of their breeding system or pollination biology (or the information is not easily available), which means we may be missing important clues explaining the causes of their rarity.And second, most of the data on pollination systems available for our work (approx.80%) is based on lists of insect visitors (sometimes as old as those of K n u t h (1898)(1899)(1900)(1901)(1902)(1903)(1904)(1905), visitation indices or anecdotic observations rather than detailed work on pollinator effi ciency.And it is generally agreed that the number of pollinators (or the list of fl ower visitors) is a poor measure of fl ower specialization and pollinator importance (W a s e r et al. 1996 ), which thoroughly explain pollination biology or breeding system of the studied plants.Unfortunately, they are in minority, the prevailing amount of data being far from complete.This means that we urgently need more studies to obtain a whole picture of the problem.

Fig. 1 .
Fig. 1.Titles, keywords and abstracts of papers from ISI Web of Science® database searched for pollination.Dotted line connects points among years and solid line is a regression line.

Fig. 2 .
Fig. 2. Key insect pollinators of 249 entomogamous plant taxa from the Polish red list.Th e number of taxa does not add to 249 as many species are pollinated or visited by, more than one insect group.Hym -bees, Dip -fl ies, Lep -butterfl ies and moths, Col -beetles.
; J o h n s o n and S t e i n e r , 2000; P e l l m y r , 2002).It has already been demonstrated by many authors (e.g.H e r r e r a , 1987; F i s h b e i n and Ve n a b l e , 1996, I v e y et al. 2003; Z y c h , 2007) that the key pollinators may constitute only a small portion of the total fl oral entomofauna.There are case studies, e.g. for Aconitum lycoctonum (U t e l l i et al. 1999; U t e l l i and R o y 2000, 2001), Drosera anglica (M u r z a and D a v i e s , 2005; M u r z a et al. 2006), Gentiana pneumonanthe (P e t an i d o u et al. 1995, 2001), Orobanche elatior (O l l e rt o n et al. 2007) or Salix lapponum (T o t l a n d and S o t t o c o r n o l a , 2001 Dipterans constitute the second important group (visits to approx.33% of the taxa).Butterfl ies and moths visit and pollinate approx.11% of the Red list plants, beetles 3%, and less than 1% is visited and pollinated by other insects Th e list of 47 plant taxa from the Polish red list for which the literature data on pollination and/or breeding system was unavailable for the authors.