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THE FRESHWATER CRUSTACEA OF YORKSHIRE

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GEOFFREY FRYER

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' T
April-June' 1998

Natur

i:„

Number 1025
Volume 123

C

A QUARTERLY JOURNAL OF NATURAL HISTORY FOR

THE NATURAL
HISTORY MUSEUM

20 JUL 1993

PURCHASED
3ENERAL LIBRARY

Introduction to the Proceedings of the Broomrape Conservation
Workshop —

Alistair D. Headley

Taxonomic Problems in the Orobanchaceae - The British
Perspective —

Fred J. Rumsey

The Status of Orobanche reticulata Wallr. in the UK —

David G. E. Knight

Monitoring of Orobanche reticulata Wallr. Populations in
Yorkshire, England —

Alistair Headley, Phyl Abbott and Michael Foley

Some Aspects of the Autecology of Orobanche reticulata Wallr. —

Alistair Headley, Michael Hughes and Mary Jeavans

Management and Conservation Status of Sites with Orobanche
reticulata Wallr. Populations —

Colin Newlands and Helen Smith

Are British Orobanche reticulata species in decline? —

Fred Rumsey and Alistair Headley

The Way Forward for Broomrape Conservation in Britain —

Alistair D. Headley, FredJ. Rumsey and lan Taylor

The Biology and Ecology of Orobanche: A Bibliographic Review

Alistair D. Headley and Fred J. Rumsey

Published by the Yorkshire Naturalists’ Union

Editor M. R. D. Seaward, MSc, PhD, DSc, FLS, The University, Bradford BD7 1DP

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INTRODUCTION TO THE PROCEEDINGS

OF THE BROOMRAPE CONSERVATION WORKSHOP

PURCHASED

compiled by GE N E R A L Li B RAR Y

ALISTAIR D. HEADLEY

THE NATURAL
HiSTORY MUSEUM

49

20 IUL 1993

Department of Environmental Science, University of Bradford, Bradford BD7 1DP

On 17 October 1997 a group of 18 out of a total of 27 invited delegates attended a one-day
workshop on the conservation of broomrapes at English Nature’s offices in Wakefield. This
is the lead office for Orobanche reticulata and the Southern Magnesian Limestone Natural
Area in which this plants distribution is centred. An informal partnership of English Nature,
David Knight of Leeds City Council, Phyl Abbott and myself was established as a
consequence of being involved in the conservation of the thistle broomrape, O. reticulata
Wallr. in Yorkshire This partnership has been working together to solve some of the
knottier problems of managing and researching the ecological requirements of this protected
• species for over three years.

It became clear from discussing issues with other organisations and individuals that the
same problems arose with other rare species of Orobanche. It was felt that the lessons learnt
from working on O. reticulata were applicable to many of the other rare or conservationally
important species of Orobanche. A workshop was organised in order to disseminate these
findings to a broader group of people responsible, in part at least, for managing sites
■ supporting these species. The intention of the workshop was not only to impart our
I knowledge of O. reticulata, but to learn from other people’s experiences in managing
Orobanche populations, and hopefully to examine ways in which the conservation and the
understanding of the ecology of this neglected group of plants could be advanced.

Broomrapes, Orobanche L., are an unusual group of plants that are holoparasitic on the
i roots of other angiospermous plants. The extant understanding of the biology of these plants
is largely derived from studies of pest species that parasitise crops, mainly in the
Mediterranean region, Africa and the Middle East. The paper given by Headley and Rumsey
(1998) gives a review of this extensive literature in so far as it is relevant to the ecology and
management of conservationally important species of broomrape. The taxonomy of
Orobanche is notoriously difficult. These problems, as well as a report on the changing
abundance and distribution of the nine species of the genus native to the British Isles were
outlined by Fred Rumsey (1998).

The workshop opened with an outline of the status of O. reticulata and background to the
conservation work by David Knight (1998). The conservation of any organism is crucially
dependent on the monitoring of its population size. The sterling monitoring work carried out
by Phyl Abbott and Michael Foley (Headley et al., 1998a) has important implications for
the conservation work described by Colin Newlands and Helen Smith (1998).

The conservation of any organism should be based on a sound knowledge of its
autecology. The most pertinent results of autecological investigations carried out by
Michael Hughes and Mary Jeavans are also given (Headley et al., 1998b). Clearly, much
remains to be done before the ecological requirements of this plant are adequately
understood, but there is the added complication that the ecology of the host plant has also to
be considered; for a common weedy species this is not as comprehensive as one would wish.

Lunch was kindly provided by English Nature, during which discussions proceeded on
the problems of monitoring other species of broomrape and the ways in which the
conservation of this group of plants could be advanced (Headley et al., 1998c). In the
afternoon, delegates visited two sites with contrasting habitats and management. The first
was at Hook Moor where Kvaerner-Balfour Beatty kindly gave permission for the group to
examine the population on the embankments of the Al near Aberford and the effects of
management on it. Here the major M 1 -A 1 link road scheme is being carried out and the full
co-operation of the constructors in avoiding any damage to the populations must be

Naturalist 123 (1998)

50

Taxonomic Problems in the Orobanchaceae - The British Perspective

commended. The group then made its way to near Collingham where David Smith and Katy
Botrell of the East Keswick Wildlife Group guided the party around Ox Close wood and
described the different experimental management regimes at the site. After further
discussion it was decided that the presentations from the meeting would be of value to
others and the following seven papers hope to go some way towards filling gaps in our
understanding of the ecology and conservation of British broomrapes.

References

Headley, A. D., Abbott, P. P. and Foley, M. J. Y. (1998a). Monitoring of Orobanche
reticulata Wallr. populations in Yorkshire. Naturalist 123: 56-60.

Headley, A. D., Hughes, M. and Jeavans, M. K. ( 1998b). Some aspects of the autecology of
Orobanche reticulata Wallr. Naturalist 123: 60-70.

Headley, A. D., Rumsey, F. J. (1998). The biology and ecology of Orobanche: a
bibliographic reviews. Naturalist 123: 89-98.

Headley, A. D., Rumsey, F. J., Knight, D. and Taylor, I. (1998c). The way forward for
broomrapes conservation in Britain. Naturalist 123: 86-89.

Rumsey, F. J. (1998). Taxonomic problems and rarity in the Orobanchaceae - the British
perspective. Naturalist 123: 50-53.

Newlands, C. and Smith, H. (1998). Management and conservation status of sites with1
Orobanche reticulata Wallr. populations. Naturalist 123: 70-75.

TAXONOMIC PROBLEMS IN THE OROBANCHACEAE -
THE BRITISH PERSPECTIVE

FRED J. RUMSEY

Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD
What are the Problems and Why?

The taxonomy of Orobanchaceae is controversial and still largely unresolved. At the outset
the recognition of the Orobanchaceae as a distinct family is an issue. Also some would treat
the Orobanche subgenera as currently recognised at a generic level. These issues apart, there
are still some intractable problems at the specific level. However, relatively few of these
difficulties relate to the small number of taxa present in the British Dora. As the British Isles
are at the north-western extremity of the distribution of this mainly Mediterranean and south-
west Asian ‘genus’, the number of species present are few and the population sizes are also
small (see below).

The widescale morphological reduction as a consequence of parasitism has limited the
number of available characters for traditional taxonomic methods. This therefore poses many
taxonomic problems in this genus, as it does for most parasitic groups. Plant stature,
pigmentation and perhaps other morphological characters depend to an unknown degree on
the host plant. This makes them unreliable as taxonomic characters. In order to test the level
of plasticity of characters and to determine what is controlled by the host and the
environment, it is necessary to carry out controlled experiments in cultivation. The parasite,
however, is often difficult to cultivate under controlled conditions. Such experiments are also
needed to establish the potential host ranges and reveal any host-preferential or host-specific
‘races’ in taxa thought to be generalist parasites.

Speciation may be host driven (Norton & Carpenter, 1998). It is possible to envisage a
situation whereby a single seed may be dispersed over a long distance and may establish
itself on a novel, but just acceptable host. Geographic isolation resulting in repeated selling,
along with strong selective pressures to grow on a particular host, novel habitats and host
plants influencing phenology, may all act to reinforce reproductive isolation. This may
eventually lead to local ‘races’ or ‘strains’ which could be considered good ‘biological

Naturalist 123 ( 1998)

Taxonomic Problems in the Orobanchaceae - The British Perspective 5 1

species’, but unless some morphological change from the ancestral stock has also become
fixed, they will not be recognised by traditional taxonomic methods. These are termed
‘cryptic species’. Host specific, or at least host preferential races, have been demonstrated to
exist in O. minor (Musselman & Parker, 1982).

Because of the lack of morphological characters and host driven plastic responses it is
possible to overlook biologically distinct lineages and, conversely, where easily observed
morphological characters are expressed, they may be given too much weighting. In the
absence of breeding programmes and cultivation, it is difficult to be sure. The development
of a range of molecular methods will undoubtedly provide additional characters and reveal
much more about the underlying genetic diversity, breeding systems and gene flow of taxa,
all of which may have a profound importance when conservation strategies are being
considered.

Taxonomic problems in British orobanche
1. O. reticulata Wallr.

The first problem, particularly pertinent given the main thrust of these proceedings, relates to
0. reticulata s. lato. Several taxa have been recognized and treated as various ranks, from
full species to varieties, including O. pallidiflora Wimm. & Grab and O. procera Koch.
Yorkshire plants have been ascribed to different segregates by different authors. As a whole,
this aggregate is morphologically quite distinct by virtue of its corolla shape and the presence
of numerous dark glands on the corolla, a feature shared by very few species. All are
parasites of the tribe Cynarae of the Compositae, perhaps also parasitising Dipsacaceae and
others in the Balkan part of their range.

Some central European authors suggest that ecological, host and general distributional
differences exist between these entities (e.g. Kreutz, 1995).

The following taxonomic questions therefore need to be addressed:

• do we have more than one taxon in the British Isles?

• to which of the recognized segregates do our plants belong?

• are these segregates good species, or what rank do they deserve?

Preliminary studies suggest that the few British populations are of a single taxon. Marked
differences in the extent of the pigmentation and to a certain extent nomenclatural confusion
may have led to the suggestion that several entities were present. British plants have the very
characteristic corolla shape and general stature of the more lowland O. procera , which Foley
(1998) suggests is best treated as a subspecies of O. reticulata. Further work is clearly
desirable to clarify this situation. However, other taxonomic issues in the genus, particularly
with the O. minor agg., should have a far higher priority.

What is of high priority with regard to O. reticulata is a survey of genetic diversity,
comparing material from the British sites with each other, within sites, within areas and with
continental material. This would make it possible to test the ideas of lower genetic variation
in the smaller populations and the idea of metapopulations within river systems (Headley et
al., 1998). It is likely that genetic variation is low in the more isolated populations, such as
Cow Cliff pasture, due to past genetic bottlenecks and inbreeding. Conversely, some
apparently small populations may maintain considerable genetic variation due to the
presence of seed banks and some outbreeding and gene flow. This has the potential to be an
exciting, small, hence achievable and yet not an overly expensive project.

2. O. minor L.

The O. minor aggregate probably poses the most difficulties within the genus, both from a
British and European viewpoint. Within Britain, four taxa have been accorded varietal rank
under O. minor s. stricto , one almost restricted to the British Isles, and for many years treated
as a species as O. maritima Pugsley. It was included in the last edition of the U.K. Red Data
Book (Perring & Farrell, 1983) and its distribution, etc. is given in Scarce Plants in Britain
(Stewart et al., 1994). This has been much confused with forms of O. minor s. stricto
growing in maritime habitats and to a lesser extent with O. picridis where they co-exist in
Kent. Old records, and some new. must therefore be treated with caution. This exclusively

52 Taxonomic Problems in the Orobanchaceae - The British Perspective

maritime taxon predominantly parasitises the south-west coastal subspecies of Daucus
carota , ssp. gummifer. This, like the parasite, is a rather weakly morphologically
differentiated taxon, split from a widespread variable species, but with a distinct ecology and
geographic circumscription. ‘O. maritima’ undoubtedly grows elsewhere along the Atlantic
seaboard of Europe as material referable to this taxon was seen growing on the Cape St.
Vincent. Portugal by the author in April 1995. Its rank may need to be re-assessed following
any molecular work. Its demotion to varietal rank was largely a pragmatic approach to the
problems of trying to differentiate it on purely morphological grounds and the very poor
herbarium specimens in most cases. Chater and Webb (1972) suggest that it may be
intermediate between the ‘minor’ and ‘artemisiae-campestris’ aggregates. There is no
evidence for this supposition.

The correct name for plants included in British floras under var. flava E. Regel requires
further research. All Orobanche species produce plants that are lacking in the purple
pigmentation which can mask any underlying paler pigmentations. Assuming this has a
genetic cause, it is possible that this character could become fixed in certain populations,
even if it is a recessive mutation, following selfing and no significant gene flow to the var.
flava population from ‘normal’ populations. Confusion with albino plants must be avoided.
The suggestions that albino plants are found growing on injured or inappropriate hosts are
based on ignorance of the mechanisms involved in plant metabolism and biosynthesis of
plant pigments.

Yellow O. minor plants have been recorded from East Anglia and scattered localities
throughout the geographic range of the normal type, but populations of these plants rarely
persist. The British locus classicus of var. flava is the St. Ouens area of Jersey. Material from
here may not be identical with most British yellow plants and are perhaps a pigment-less
form of var. maritima. Though widely collected last century, similar plants have not been
seen at this locality for over 50 years. Superficially similar plants still grow in the Newport
Docks, Gwent and this population warrants further investigation.

O. minor var. compositarum Pugsley is a rather poorly defined taxon, separated on weak
morphological grounds. Its distribution is unclear, most particularly its extra-British range, as
most continental authors have not recognised or accepted it. It appears that Pugsley (1940)
described it to accommodate plants of O. minor that approached O. picridis in some
characters, and could be found on similar composite hosts. The narrow sub-erect corollas
which typical material of this variety shows can, however, be found on plants parasitising
legumes. Changes in corolla attitude occur in most plants of O. minor after anthesis and
during seed maturation, such that the corollas are eventually somewhat sub-erect. It is
suspected that this taxon has become something of a nomenclatural dustbin for specimens
that do not fit neatly into a clear taxon; it is doubtful that it is worthy of recognition at
varietal rank, but again work is needed before such a conclusion can be reached.

The typical variety of O. minor is a very variable plant, and as populations tend to be
ephemeral, it makes it difficult to re-examine the consistency of characters within a
population from year to year, let alone in individuals. It is considered to be an introduction in
Ireland and much of central Europe and may well be so in Britain. A more convincing case
for native status could be argued for O. minor var. maritima. Many areas in southern Europe
have morphologically distinct and often host preferential races, where this taxon s. lato is
more or less uniform; for example, in Mallorca plants primarily parasitize Galactites
tomentosa and have a distinctive appearance, approaching another poorly known segregate
O. calendulae Pomel in appearance. In Britain it can be hypothesized that populations of O.
minor are survivors of repeated introductions from diverse sources elsewhere in its range.
Cleaner seed and greater pesticide use over the last 40 years or more have slowed this input.
A limited range of the genetic diversity present in this species may have been imported, i.e. a
few strains particularly associated with definite crop hosts, such as Trifolium spp. The source
populations were probably geographically isolated prior to their introduction to Britain, and
the subsequent hybridization would create new patterns of diversity in morphology and host
range. The possibility of hybridization with other taxa should also be considered, and indeed

Taxonomic Problems in the Orobanchaceae - The British Perspective 53

specimens that suggest possible hybridization between O. minor and O. picridis, O.
reticulata and O. crenata have been observed. The artificial hybrid O. minor x O. reticulata
was made by Mike Jones, demonstrating the possibility of such a cross (Jones, 1989).
Furthermore, chromosome counts of some Mediterranean taxa would indicate that
polyploidization has played a role in broomrape speciation (Valdes et ai, 1987). Whether
these tetraploids are of an auto- or allopolyploid nature remains to be determined.

3. O. hederae Duby

One other taxa in the O. minor aggregate of concern from a British perspective is O. hederae
Duby. This is a widespread and predominantly western parasite of ivy, especially the
tetraploid Hedera hibernica. O. hederae differs in small, but more or less constant
morphological characters from O. minor and has only ever reliably been recorded
parasitizing members of the Araliaceae, whereas O. minor has rarely been found on Hedera.
It is still questionable whether O. hederae should be given specific or subspecific rank, given
the small morphological differences between it and O. minor.

4. O. artemisiae-campestris Vaucher

O. artemisiae-campestris resembles O. minor in being an aggregate of closely related,
morphologically poorly distinguished taxa. This has been compounded by nomenclatural
wrangling as the laws of priority despatch well known names, adding to confusion.
Vaucher’ s name should in any case be rejected as a polynomial as the hyphen does not
appear in the original publication (Vaucher, 1827). This is not just a lapse as he consistently
used polynomials derived from suspected hosts to name his taxa. The British O. artemisiae-
campestris is of the taxon which most central European authors accept at species rank as O.
picridis F. W. Schultz. This was the name used in earlier British floras, but was found to be
pre-dated if the taxa were treated in an aggregate sense, first by O. loricata, then the
atrocious O. artemisiae-campestris. This latter taxon, in its restricted sense, is a parasite of
Artemisia campestris and is much more geographically and ecologically restricted than O.
picridis, which finds its northern-most limit in Britain. The proximity of O. minor s. lato in
the Kent sites may be cause for concern if indeed the two do hybridize. Further work is
clearly needed here.

References

Chater, A. O. and Webb, D. A. (1972). Orobanche, in T. G. Tutin et al. (eds.) Flora Europea,
Vol. 3. Cambridge University Press, Cambridge.

Foley, M. J. Y. (1998). Taxonomic problems in European members of the genus Orobanche
L. Ph.D. thesis, University of Lancaster, Lancaster.

Headley, A. D., Abbott, P. P. and Foley, M. J. Y. (1998). Monitoring of Orobanche
reticulata Wallr. populations in Yorkshire. Naturalist 122: 56-60.

Jones, M. (1989). Taxonomic and ecological studies in the genus Orobanche L. in the British
Isles. Ph.D. thesis, University of Liverpool, Liverpool.

Kreutz, C. A. J. (1995). Orobanche. The European Broomrape Species. Vol. I: Central
Europe and Northern Europe. Stichting Natuur, Limburg.

Musselman, L. J. and Parker, C. (1982). Preliminary host ranges of some strains of
economically important broomrapes ( Orobanche ). Economic Botany 36: 270-273.

Norton, D. A. and Carpenter, M. A. (1998). Mistletoes as parasites: host specificity and
speciation. Trends in Ecology and Evolution 13: 101-105.

Perring, F. H. & Farrell, L. (1983). British Red Data Books, 1. Vascular Plants. 2nd ed.
Lincoln.

Pugsley, H. W. (1940). Notes on Orobanche L. Journal of Botany 78: 105-1 16.

Stewart,' A., Pearman, D. A. and Preston, C. D. (1994). Scarce plants in Britain.
Peterborough.

Valdes, B., Talavera, S. and Fernandez-Galiano, E. (1987). Flora vascular de Andalucia
Occidental 2. Barcelona.

Vaucher, J. P. ( 1 827). Monographic des Orobanches. Geneva.

54

THE STATUS OF OROBANCHE RETICULATA WALLR. IN THE
U.K. AND THE BACKGROUND TO THE WORK CARRIED OUT
UNDER THE SPECIES RECOVERY PROGRAMME

DAVID G. E. KNIGHT
Conservation Section , Leeds Leisure Services,

Leeds City Council, The Town Hall, The Headrow, Leeds LSI 3 AD

Thistle broomrape ( Orobanche reticulata Wallr.) is a rare plant of limited distribution
within Britain and is classified as ‘endangered' in the British Red Data Book of Vascular
Plants. It is listed in schedule 8 of the Wildlife and Countryside Act 1981 and is
accordingly afforded legal protection under section 13 of the same Act. A number of Sites
of Special Scientific Interest have been designated either solely or partly because of the
presence of this species.

In Britain, thistle broomrape is confined to Yorkshire, and is largely restricted to the
narrow strip of magnesian limestone within it (Fig. 1). Such a distribution would seem to
make it a suitable species for championing or adoption by Yorkshire natural history or
nature conservation bodies. However, like other British broomrape species, the profile of
thistle broomrape has, hitherto, not been commensurate with the species’ conservation

FIGURE I

Map based on Foley (1993) showing the distribution of Orobanche reticulata in Yorkshire
in relation to the major rivers and the band of magnesian limestone (shaded area).
Solid circles represent extant localities in 2 km x 2 km squares and
crosses represent colonies presumed extinct.

Naturalist 123(1998)

55

The Status o/ Orobanche reticulata in the U.K.

status. Although it is listed with proposed targets for its conservation in ‘Biodiversity
Challenge’ (Anon., 1993), it is not listed in the sequel, ‘Biodiversity Challenge (second
edition)’ (Anon., 1994), and within ‘Biodiversity: The UK Steering Group Report, Volume
2: Action Plans’ (Anon., 1995) it appears only on the ‘long list’ of 1,250 species, along
with bluebell ( Hyacinthoides non-scripta ), great tit (Parus major) and roe deer ( Capreolus
capreolus).

There are a number of aspects of the species which make it ‘difficult’ and undoubtedly
contribute to its apparent low ranking in terms of conservation concern. Firstly, O.
reticulata was not discovered as a British species until 1907. This in itself reflects
difficulties in the identification and taxonomy of the genus Orobanche, many of which still
await clarification and resolution (Rumsey, 1998). It also means that there is no reliable
body of historical records against which contemporary distributions can be compared.

Secondly, because of its parasitic nature, the plant appears only as a flowering spike
during the summer months. Although the dead spikes frequently persist through the winter
months, the living plant is ephemeral, and opportunities to see it in the field fully
developed, in a reliably identifiable state, are limited.

As a parasite of thistles, and particularly creeping thistle ( Cirsium arvense ), thistle
broomrape grows in greatest concentrations in the vicinity of thistle stands, making
thorough surveying and monitoring an uncomfortable experience! These thistle stands are
often within Arrenatheretum elatioris grassland (Hughes & Headley, 1996), a vegetation
type of negligible interest to naturalists and conservationists alike. A further disincentive is
provided at Hook Moor, a key site for the species, where thistle broomrape is found on
steep road embankments at a junction on the Al.

A further problem arises from the wide fluctuations in numbers of plants to be found at
sites from year to year and the sudden appearance of flowering spikes after years of
apparent absence.

In view of the above difficulties, it is perhaps not surprising that, prior to the Species
Recovery Project, very little was known about the ecology of thistle broomrape. It was this
lack of information that prompted the establishment of the project, when in 1993 tree and
scrub encroachment at Hook Moor seemed to pose a threat to the long-term viability of the
broomrape population.

Although the project initially concentrated on monitoring population changes in response
to site management, it also initiated the first comprehensive surveys for the species. It has
subsequently expanded to include a programme of monitoring for key sites; the
establishment of fixed experimental management plots; and a growing programme of
research into many key areas of the species’ ecology. A Species Action Plan has been
produced and the partnership of organisations involved in the project publish an annual
newsletter to raise awareness about the species and report on the progress of the project and
the latest research findings. From the initial handful of enthusiasts, the conservation of
thistle broomrape has grown to capture the interest of literally hundreds of people - the
newsletter has a national distribution list and a print run of over 200.

The project partnership is grateful to English Nature for its financial assistance, and the
commitment of a further three years’ grant aid. Although ongoing resourcing of the project
is still challenging, the project has achieved significant success in raising awareness and
increasing understanding of thistle broomrape as well as achieving the management of key
broomrape sites.

Perhaps the work of the partnership between English Nature, various landowners, Leeds
City Council, Yorkshire Wildlife Trust, East Keswick Wildlife Trust and the University of
Bradford could provide a model for dealing with issues concerning the genus Orobanche as
a whole.

References

Anon. (1993). Biodiversity Challenge. H.M.S.O.

Anon. (1994). Biodiversity Challenge. Second edition. H.M.S.O.

56 Monitoring o/Orobanche reticulata Populations in Yorkshire

Anon. (1995). Biodiversity: The UK Steering Group Report, Volume 2: Action Plans.
H.M.S.O.

Foley, M. J. Y. (1993). Orobanche reticulata Wallr. populations in Yorkshire (north-east
England). Watsonia 19: 247-257.

Hughes, M. and Headley, A. D. (1996). The biology and ecology of the thistle broomrape,
Orobanche reticulata Wallr. Naturalist 121: 3-9.

Rumsey, F. J. (1998). Taxonomic problems in the genus Orobanchaceae - the British
perspective. Naturalist, pp. 12 2: 50-53.

MONITORING OF OROBANCHE RETICULATA WALLR.
POPULATIONS IN YORKSHIRE

ALISTAIR HEADLEY

Department of Environmental Science, University of Bradford, Bradford BD7 l DP

PHYL ABBOTT
73 Ridgeway, Leeds LS8 4DD
AND

MICHAEL FOLEY

Department of Biological Sciences, Institute of Environmental and Natural Sciences,
University of Lancaster, Lancaster LA I 4YQ

History of Recording

The monitoring of Orobanche reticulata Wallr. populations is the most comprehensive for
any of the species of broomrape in the British Isles. The site with the longest continuous
period of recording and monitoring is that at Ripon Parks in North Yorkshire. The counting
was carried out initially over many years by Mrs Janet Deane, a secretary to the Ministry of
Defence establishment that owns the land at Ripon Parks and surrounding land. With the
exception of 1989, all 14 years of recording have been covered since recording started in
1984. A complete survey of all the North Yorkshire sites was carried out in 1992 (Foley,
1992) and of all sites in West Yorkshire in 1994 and 1995 (Abbott, 1994, 1995). It w'as not
until 1996 that all 27 extant sites were surveyed (Abbott, 1996). Some sites have had
intermittent comprehensive or partial surveys of the number of flowering spikes in the
1980s and early 1990s (Abbott, 1991). This includes Quarry Moor, Hook Moor, Linton
Common, Keswick Fitts, Carthick Wood and Hetchell Wood. Foley (1993) gives details of
the distribution of the species, including the loss of O. reticulata from at least three sites in
Yorkshire since it was first collected.

Methods

The surveying of populations by Abbott and Foley has been carried out using a 1:10,000
scale Ordnance Survey map for locating the colonies and a standard N.C.C. rare species
recording sheet. These are used to help draw sketch maps of the position of individual
spikes or groups of spikes at the sites, which are carefully walked up and down to ensure
all the potential ground is covered. The time of year at which monitoring is carried out is
important: if it is carried out too early, spikes which emerge late in the growing season will
be missed and if carried out too late some or all spikes at a site may be destroyed or
removed by flooding, ploughing or mowing. Since O. reticulata grows in tall herbaceous
vegetation, Abbott carried out the monitoring in October when the tall Arrhenatherum and
Urtica had largely died down. This reduced the likelihood of missing spikes in this type of
vegetation. There is, however, the possibility of spikes at sites on the banks of the rivers
Ure and Wharfe being washed away by autumn floods.

Naturalist 123(1998)

57

Monitoring o/Orobanche reticulata Populations in Yorkshire

Results and Discussion
Broomrapes are notorious for showing large inter-annual fluctuations in population size,
but are reasonably faithful to particular sites for most species. The results of the monitoring
ol the population size for four different O. reticulata sites with the longest periods of
recording are shown in Figure 1. This clearly illustrates the large inter-annual variation in
population size in all sites covered which are in some cases over three orders of magnitude.
This results in arithmetic means of population size over-estimating the effective size of a
population; for example, taking the average number of spikes recorded for all sites and
years gives a mean value of 63, yet the actual median value is 12.5 spikes per population.

It is therefore recommended that the harmonic mean is calculated from the annual totals
to give a realistic estimate of the effective population size of any particular population of
broomrape (Caughley & Gunn, 1996). Table 1 shows the arithmetic and harmonic means
for the sites with at least four years of data. The harmonic mean, Neg, is calculated using
the following formula, where is n is the number of years the population was censused and
Ni is individuals recorded in the zth year.

n

Neg~n tX(1 tM')
i=i

If there is a year without any individuals it is necessary to add one to each year’s
population size before taking the reciprocal. If this is carried out, one has to be subtracted
from the the final value obtained at the end.

TABLE 1

The range, arithmetic and harmonic means of the number of flowering spikes of
Orobanche reticulata at the largest and mostly frequently monitored sites in Yorkshire.

Site

number of
years

range

arithmetic

mean

harmonic

mean

Nunwick meadow

3

35- 113

71

57

Ox Close Wood

5

12-787

348

54

Hook Moor

9

12-555

232

53

Cow Cliff pasture

11

0->1000

153

23

Hetchell Wood

9

3-47

14

7

Ripon Parks

13

1-748

78

5

Keswick Fitts

8

6-74

25

5

Quarry Moor

8

0-81

19

2

Linton Common

8

0-34

9

2

The results of this analysis show that only three sites have effective population sizes of just
over 50 spikes. According to the 50/500 minimum viable population rule (Frankel & Soule,
1981), these populations stand a 95% probability of surviving for 100 years. The other sites
are more likely to suffer significant inbreeding (>1%) and consequent loss of genetic
variation. This principal, however, probably does not apply to a plant that relies on a
persistent and probably large dormant seed bank for recruitment.

Figure 1 shows that there are no consistent patterns between years across sites; for
example, 1995 was a hot, dry summer, but it did not result in peak numbers of flowering
spikes across all sites. This suggests that climate is not a primary and over-riding factor
controlling flowering in this species. Statistical tests were carried out to examine whether

58

Monitoring o/Orobanche reticulata Populations in Yorkshire

Year
FIGURE 1

Changes in the flowering population size (number of spikes) of four populations of

Orobanche reticulata in Yorkshire.

the number of flowering spikes at three O. reticulata sites (Hook Moor, Cow Cliff pasture
and Ox Close Wood) were related to selected climatic variables (monthly mean minimum
and maximum temperatures, monthly precipitation, monthly number of dry days and total
monthly hours of sunshine) collated from the nearest meteorological station (Durham). The
results of this analysis showed that none of the climatic variables in the summer had a
significant effect on the population size. There are, however, significant positive
correlations between increasing September precipitation and the size of the Cow Cliff
pasture population, January precipitation and the Ox Close Wood population, and a
significant negative correlation between April precipitation and the size of the Hook Moot-
population.

Given the distribution of sites of O. reticulata in Yorkshire along the banks of the rivers
Ure and Wharfe and the small size of the seeds, it is likely that there is considerable input
of seeds downstream along these notoriously ‘flashy’ watercourses. Thus one might
suggest that the many small populations along the rivers are effectively two larger and
more widely dispersed populations or metapopulations with occasional exchange of genetic
information between the sub-populations along the banks of the river (Fig. 2). If this is the
case then there are effectively between 6 and 8 populations in the whole of Yorkshire:
Hook Moor, Cow Cliff pasture, Hetchell Wood, R. Wharfe, R.Ure and Quarry Moor. Ox
Close Wood and Linton Common are well above the flood-plain of the river Wharfe, yet
are very close to extant populations along the banks of the Wharfe and may therefore act as
source populations.

Although it would be ideal to determine the number of tubers present at certain sites in
order to ascertain the proportion of those that flower, such a procedure would be highly
destructive. It might be argued that the number of flowering spikes is not a reliable means
of determining population size as many tubers may not flower each year and perennate one
or more years before flowering. However the number of flowering spikes and hence seed

Monitoring o/Orobanche reticulata Populations in Yorkshire

59

FIGURE 2

Map showing the location of populations of Orobanche reticulata in Yorkshire in relation
to the rivers Wharfe and Ure and their effective size based on harmonic means of the

number of flowering spikes.

output is the most important determinant in maintaining and replenishing the seed bank

which is almost certainly the key factor in the persistence of any population.

Conclusions

• Counting flowering spikes is the only effective way of estimating population sizes of
broomrapes.

• Monitoring of populations by counting flowering spikes infrequently may over- or
under-estimate the size of a population due to the large inter-annual variation in
flowering.

• Counting flowering spikes at the end of the flowering season is recommended to avoid
missing flowering spikes that emerge late in the season.

• Calculating the average size of the flowering population of broomrapes using arithmetic
means over-estimates the effective population size and the calculation of the harmonic
mean is strongly recommended.

• The number of effective populations of O. reticulata could easily be much lower than the
number of recorded sites due to metapopulation dynamics whereby much smaller sink
populations are only maintained by significant dispersal of the minute seeds down rivers
from larger source populations.

References

Abbott, P. P. (1991, unpubl.). Orobanche reticulata in West Yorkshire. English Nature,
Wakefield.

60 Some Aspects of the Autecology of Orobanche reticulata

Abbott, P. P. (1994, unpubl.)- Orobanche reticulata in West Yorkshire. English Nature,
Wakefield.

Abbott, P. P. (1995, unpubl.). Orobanche reticulata in Yorkshire. Leeds City Council,
Leeds.

Abbott, P. P. (1996, unpubl.). Orobanche reticulata in Yorkshire. Leeds City Council,
Leeds.

Caughley, G. and Gunn, A. (1996). Conservation Biology in Theory and Practice.
Blackwell, Oxford.

Loley, M. J. Y. (1992 unpubl.). Survey for Orobanche reticulata (thistle broomrape ) in
North Yorkshire. English Nature, York.

Loley, M. J. Y. (1993). Orobanche reticulata Wallr. populations in Yorkshire (north-east
England). Watsonia 19: 247-257.

Frankel, O. H. and Soule, E. (1981). Conservation and Evolution. Cambridge University
Press, Cambridge.

SOME ASPECTS OF THE AUTECOLOGY OF
OROBANCHE RETICULATA WALLR.

ALISTAIR HEADLEY

Department of Environmental Science , University of Bradford, Bradford BD7 1DP

MICHAEL HUGHES

Department of Geography, University of Leicester, Leicester

AND

MARY JEAVANS

English Nature, Genesis Building 1, Science Park, University Road,
Heslington , York YOI 5DQ

Introduction

Our knowledge of the biology and ecology of broomrapes is heavily biased towards those
which are serious crop pests in the Mediterranean, Africa and North America (Headley &
Rumsey, 1998). This has meant the biology of infection of crop plants has been intensively
studied and other aspects of the life-cycle, especially in non-pest species, is sadly lacking.
An examination of certain aspects of the ecology of broomrapes was covered by Jones
(1989), but again this is limited in its coverage of the ecology and biology of the rare
broomrapes which is critical to their conservation. Michael Hughes initially examined the
biogeography of O. rapum-genistae and O. elatior using GIS in an undergraduate
dissertation in 1994/95 (Hughes, 1995a) and later carried out an autecological examination
of O. reticulata with help from the College and Environment Link (CEL) scheme. It was
clear from this work that factors governing germination of O. reticulata seeds and their
infection of host plants was the critical stage governing population sizes of this plant. This
was taken up by Mary Jeavans as an undergraduate project on the seed biology of O.
reticulata in 1995/96 (Jeavans, 1996) which was extended into the late summer and
autumn of 1996 with funding from the Species Recovery Programme.

The general biology and ecology of Orobanche is given by Headley and Rumsey ( 1998);
broomrapes are, however, root holoparasites of a wide variety of mainly dicotyledonous
plants (Krcutz, 1995). This means that their life-cycle is somewhat different to most
angiosperms and it is summarised in Figure I with the critical processes and factors
thought to be important in controlling population size indicated.

Naturalist 123(1998)

Some Aspects of the Autecology o/Orobanche reticulata 6 1

SEED (burial)

(italics) in the transition from various stages (capitals).

Results and Discussion
Geology and Soils

Although many sites for O. reticulata are found on magnesian limestone in Yorkshire,
many of them are on deep layers of river or glacial alluvium in the flood-plains of rivers or
other soil types (Table 1). The soils vary from undifferentiated alluviums to rendzinas and
calcareous brown earths.

TABLE 1

The Total Number of Sites and their Conservation Status
with different Lithologies and Soil types.

Lithology

Soil Type

Total No.
of sites

No. of
SSSIs

No. of
Reserves

Magnesian limestone

calcareous brown earth

6

4

2

Magnesian limestone

rendzina

1

1

1

Chalk

rendzina

1

1

0

Fluvio-glacial deposit

alluvium

19

6

1

The texture of the soils where the plant is found today is typically a sandy loam or sandy
soil. Despite being sandy the soils are calcareous with low to moderate amounts of total
nitrogen and plant-available potassium and phosphate (Table 2). The restriction of the plant

62

Some Aspects of the Autecology of Orobanche reticulata

to particular soil characteristics might well be a reflection of the suitability with which a
whole set of conditions make it possible for the parasite to infect its exceedingly common
host plant, Cirsium ar\'ense.

The restriction of O. reticulata largely to soils with a high pH (Table 2) is perplexing as
the parasite is not dependent on the soil for any of its nutrients and its host plants are
widespread on a wide range of soil types. It is possible to generate a number of hypotheses
for such a relationship. These include (a) the higher pH soils may make the host thistles
elicit the correct stimulus for germination of the O. reticulata seeds, or (b) it may make the
host plant more susceptible to infection, or (c) these soils have factors, such as large
populations of rabbits, which are correlated with calcareous sandy soils which then makes
them suitable for establishment of this parasite on its host plant.

The concentrations of major plant nutrients in the soil are at the lower end of the range
normally found in soils (Allen et ai, 1989). This is particularly the case for total nitrogen
and exchangeable potassium. Not suprisingly, the concentrations of calcium are at the top
of the range and are typical for soils derived from a calcareous bedrock. Low nutrient
status soils and hence nutrient stressed plants are allegedly more susceptible to infection by
parasitic plants in sub-tropical areas, but this has yet to be tested with any of the British
species of broomrape.

TABLE 2

Some characteristics of 19 soil samples collected from 14 of the extant
Orobanche reticulata sites in Yorkshire.

Soil Characteristic

Range

Mean ± S.E.

PH

4.9 -8.0

7.4 ± 0.2

total nitrogen (% dry wt.)

0.04 - 0.79

0.30 ± 0.04

plant-available phosphate (ppm)

3.5-28.1

1 1.9 ± 1.6

exchangeable potassium (ppm)

3.74-45.5

13 ±2.5

exchangeable-calcium (ppm)

750-7,500

3,200 ± 300

Vegetation Type

The plant is found in two main types of vegetation (Hughes & Headley, 1996). Most sites
are grasslands of the Arrhenatheretum elatioris type (MG I of the National Vegetation
Classification or NVC). This very common grassland is the type of community in which
O. reticulata occurs on the banks and flood-plains of the rivers Ure and Wharfe. It is,
therefore, not suprising that the Urtica dioica sub-community (MG lb) is present at these
sites due to the relatively high nutrient status of the soil. At Hook Moor, however, the
community is more species-rich and can be placed in the Centaurea nigra sub-community
(MGle) of the Arrhenatheretum. The woodland sites at Hetchell and Ox Close woods are
of the Fraxinus excelsior-Acer campestre-Mercurialis perennis woodland community
(W8). However, O. reticulata is found in the clearings within the woodland sites where the
understorey is typically dominated by Mercurialis perennis and it has a greater affinity to a
Rubus fruticosus-Holcus lanatus understorey community (W24).

Seed Output

Spikes of O. reticulata have approximately 50 flowers per spike and there are about 1,000
to 2,000 seeds per capsule (Hughes & Headley, 1996). This means that the seed output of
O. reticulata, like other broomrapes, is very large (Salisbury, 1942) and is in the order of
100,000 to 200,000 per flowering spike. The seeds are small (0.17 x 0.27 mm) and thus
easily dispersed in air, water and mud or dust, by animals and humans. Thus, the

63

Some Aspects of the Autecology o/Orobanche reticulata

distribution of broomrapes could represent the random dispersal of seeds over long
distances by various agents, including humans, rather than a reflection of a set of specific
abiotic and biotic factors which provide the correct niche for the species. The clear
association of this species with the magnesian limestone area of Yorkshire counters this
argument to a certain extent.

Seed Germination

Germination of the seeds of O. reticulata was achieved after pre-conditioning them for 6
days at 25°C on moist filter paper in the dark (Brown et al., 1951; Sunderland, 1960;
BarNun & Mayer, 1993). Extracts of fine roots of C. arvense stimulated germination at
temperatures between 10 and 25°C, but the optimum temperature for germination was
found to be 15°C (Headley & Jeavans, 1996). The seeds take between 14 and 45 days to
reach maximum germination, depending on the temperature (Headley & Jeavans, 1996).
Although all the experiments presented here were carried out in the dark, it was found that
light did not inhibit germination in a few petri dishes that were accidentally left out on a
bench.

Extracts from roots greater than 5 mm in diameter did not stimulate any germination, nor
did gibberelic acid or a linseed root exudate which has been found to contain strigol by
BarNun & Mayer (1993). There is a general decline in the germination of the seeds with
increasing size of the C. arvense plant from which the fine root extract was taken (Fig. 2).

Height of Cirsium arvense plant (cm)

FIGURE 2

The mean germination (% of seeds with embryos) of Orobanche reticulata seeds
treated with 1% aqueous extracts of fine roots (diameter < 0.5 mm) taken from
Cirsium arvense plants of different heights (cm). Means of at least 150 seeds with
embryos and bars represent standard errors.

64

Some Aspects of the Autecology 0/ Orobanche reticulata

Unfortunately, the trend is not significant due to the largest C. arvense plants stimulating
the highest germination of O. reticulata seeds (Fig. 2). The field observations that O.
reticulata is not found in the tallest and densest stands of C. ar\’ense (Table 3) lends
support to the hypothesis that it is young thistle plants that are more often parasitised.
However a number of alternative explanations can be given for the observations in Table 3.
It is possible that where there is disturbance, new roots are produced by existing thistles or
that the opening out of the surface allows Orobanche seeds to reach the soil surface and
thus be washed into the rooting zone, as opposed to being stuck on a mat of leaf litter.
Whatever is the most appropriate explanation for this phenomenon, it appears that
maintaining a relatively open sward with areas of bare soil is almost certainly beneficial for
the establishment of thistle seedlings and roots for infection by O. reticulata.

TABLE 3

The density (m 2) and mean height (cm) of all Cirsium arvense plants in 1 m2 plots with
or without the parasite Orobanche reticulata. C. arvense plants that were being
parasitised by one or more spikes of O. reticulata were excluded from the observations.
Parasitised Cirsium arvense plants have a mean height of 26 cm.

Cirsium

arvense

Orobanche

reticulata

n

range

mean
± S.E.

t-test

height (cm)

present

1 17

4- 145

60 ±3

16.15

absent

173

9- 165

1 16 ±2

P<0.0()1

density (m 2)

present

13

4-20

9 ± 1.4

2.26

absent

13

6-19

13.2 ± 1.2

P<0.05

There is a highly significant effect of the species of thistle from which the root extract is
taken in affecting germination of O. reticulata seeds (Fig. 3). The two commonest species
of thistle, C. arvense and C. vulgare, stimulated the greatest germination, with lower rates
for other species of Cirsium and Carduus. This observation confirms field observations in
1995 that only 4 out of 414 O. reiculata appeared not to be parasitising C. arvense. With
the exception of C. vulgare , this might in part reflect the relative abundance of the different
host species. It does not however explain why the perennial C. ar\>ense is parasitised more
often than the equally common biennial C. vulgare. Although extracts of thistle roots does
not necessarily mean that the intact plant will necessarily be susceptible to infection by the
O. reticulata seedlings or that the correct stimulant is exuded from the roots in the correct
quantity.

The presence of a significant correlation between the number of spikes at the Cow Cliff
pasture site and the total rainfall for September of the previous year suggests that the life-
cycle might in fact be annual (Fig. 4). This is supported by pot grown plants of other
British Orobanche normally emerging within a year of being sown. The requirement for a
relatively warm moist soil for satisfactory pre-conditioning of O. reticulata seeds provides
a mechanistic explanation for the relationship shown in Figure 4. The satisfactory
establishment of thistle seedlings and/or thistle root growth may also be a factor in this
relationship.

The seeds of O. reticulata from the Hook Moor population germinated on a wider range
of thistle root extracts than seeds taken from the Hetchell Wood population. This might
imply that the seeds from the Hook Moor population have a greater potential genetic
variation. This is likely to be the case given the much smaller effective population size and
hence higher probability of selling and consequent inbreeding of the Hetchell Wood
population (Headley & Jeavans, 1996).

Some Aspects of the Autecology o/Orobanche reticulata

65

Cirsium vulgare

Cirsium

arvense

Cirsium

palustre

Cirsium

eriophorum

Carduus crispus

Carduus nutans

U Hetchell Wood
□ Hook Moor

1 1 1 1 1 r

0 20 40 60 80

100

Mean Germination (% of seeds with embryos)

FIGURE 3

The mean germination (% of seeds with embryos) of Orobanche reticulata seeds
from either Hetchell Wood (shaded bars) or Hook Moor (open bars) treated with
1% aqueous extracts of fine roots (diameter <0.5 mm) taken from 3 week old seedlings
of different species of thistle. Means of at least 150 seeds with embryos and bars

represent standard errors.

The radicles of O. reticulata died once they reached 2 mm in length, which is
presumably due to exhaustion of the carbohydrate reserves in the seed. Thus seeds of
broomrapes must germinate immediately next to the root of their potential host plant. The
germinability of the seeds kept in a laboratory at room temperatures lost only 30% of their
germinability over a 10 year period (Fig. 5). Seeds kept at the Millenium Seed Bank at
Kew Royal Botanic Gardens had lost 35% of their potential germinability over only a 3
year period (Fig. 5).

Seeds collected from herbarium specimens that were between 42 and 1 1 8 years old did
not germinate, but some seeds from an eight year old herbarium specimen did germinate
(Fig. 5). Although the seeds from old specimens did not germinate, they still had viable

66

Some Aspects of the Autecology 0/ Orobanche reticulata

FIGURE 4

Scatter plot of logarithm of population size (number of flowering spikes +1 ) of Orobanche
reticulata at Cow Cliff pasture and the total September precipitation (mm) recorded at the
nearest available meteorological station (Durham) in the previous year. 90.2% of the
variation in population size is accounted for by following equation:

Ln no. of spikes + I = 3.2025 + 0.0171*September ppt - 0.2013*0ctober max. temp.
Numbers next to points indicate year in which census was undertaken.

embryos present, as detected using a fluorescein stain (Pritchard, 1985). There is every
possibility such herbarium specimens require a longer pre-conditioning period before they
will germinate. The implications of this are profound in suggesting that sites where
broomrape spikes have not been seen for many years could be resurrected from a dormant
seed bank being present in the soil. The seeds of other broomrapes have been estimated to
have a longevity in the soil of up to 100 years. This may well have happened at the Ox
Close Wood site (Newlands & Smith, 1997; Smith and Bottrell, pers.comm.). It may also
be possible to resurrect plants with ‘old genomes’ with seeds from old herbarium
specimens from extant or extinct sites.

Seed Bank

If the chances of an Orobanche seed coming into contact with its potential host root is the
governing factor in determining the size of the flowering population of a broomrape, then it
will be the density of broomrape seeds and host roots in the soil that will determine this
chance event. For this reason an attempt was made to assess the size of the seed bank of O.
reticulata at a number of its key sites. The man-power required for the comprehensive
sampling, mechanical extraction and counting of the size of the seed bank at a large
number of sites is not feasible. An indirect estimate of the presence of a seed bank may,
however, be established by growing potential host plants in soils collected from extant or
extinct sites.

Some Aspects of the Autecology o/Orobanche reticulata

67

Seed age (years)

FIGURE 5

The effect of seed age (years) on mean germination (% of seeds with embryos) stored
in either the laboratory at room temperature (squares) or at the Kew Millenium seed bank
(-20°C and 10% humidity) or from a herbarium specimen kept at Leeds City Museum.

Seeds were extracted from 10 out of the 20 soil samples processed. The numbers varied
from 1 to 313 with a median of 5 extracted for those samples where seeds were recovered.
Considering the large spatial heterogeneity in seed numbers in the soil it was suprising to
find that there is a reasonably close relationship between the mean number of seeds
extracted out of a soil sample and the harmonic mean of the number of flowering spikes at
the same site (Fig. 6). This relationship is not suprising as the size of the seed bank will
depend on the number of flowering spikes that have been produced over many years as the
seed bank is cumulative given the likely longevity of the seeds. The feedback loop between
flowering and seed bank size indicated in Figure 1 also supports the supposition that the
number of flowering spikes produced is dependent on the probability that O. reticulata
seeds will encounter a thistle root. Therefore to increase the population at a site the number
of thistle plants and/or the size of O. reticulata seed bank need to be maximised.

Flowering

Despite the circumstantial evidence it is not certain how long it takes for O. reticulata to
complete its life-cycle in situ. Although it is monocarpic the vast majority of the time, a
single herbarium specimen had clearly produced spikes in two different years (Rumsey
pers. comm.). Also spikes that had been cut early in the summer in a strip of set-aside land
produced replacement flowering spikes within three weeks of being mown (Hughes,
1995b).

The flowering shoots of broomrape emerge rapidly from the soil, primarily by the
expansion of pre-formed cells. This is achieved by the accumulation of high concentrations

68

Some Aspects of the Autecology 0/ Orobanche reticulata

FIGURE 6

The size of the Orobanche reticulata seed bank (in mean number of seeds per 0.25 kg soil)
and effective population size of Orobanche reticulata flowering spikes
(harmonic mean) at 9 sites in Yorkshire. Spearmans rank correlation between the
two variables (rs = 0.85) is significant at the 1% level.

of sugars taken from the roots of the host plant. The flowering of O. reticulata starts in late
June to early July. Spikes continue to emerge through July, but individual flowers and
flowering spikes set seed within a few weeks. The majority of flowers have died by the end
of July, but the occasional spike can emerge late in the season. It is not certain how long
the capsules and seeds take to ripen but it is not until September that the majority of
capsules are fully ripened.

Pollination

Although wasps and a wide variety of bees have been observed to visit the flowers of O
reticulata (Jones, 1989) it is not certain whether any of these insects actually affect
pollination (Ollerton, pers. comm.). The flowers are almost certainly self-compatible and it
seems that the flowers affect self-pollination by mechanical means (Rumsey, pers. comm.).

Conclusions

Despite the amount of work carried out on this species of broomrape there are many
aspects of the ecology of the plant that are not known. This is partly a reflection of the fact
that a large part of their life-cycle is underground and therefore makes it difficult to study.
The same is true for other parasitic and saprophytic plants which only produce their flowers
above-ground, such as Lathraea squamaria, Neottia nidus-avis, Corallorhiza trifda,
Epipogium aphyllum, Monotropa hypopitys, Botrychium and Lycopodium gametophytes
and Cryptothallus.

Some Aspects of the Autecology of Orobanche reticulata 69

The factors that may be limiting the population size of O. reiculata are considered to be

the following:

• Size of the seed bank in the soil, (very variable from <1 to 313 per 250 g soil).

• The density of host roots in the soil, which will be affected mainly by the size of the host
population and soil nutrient status.

• The presence of the correct stimuli for germination of the Orobanche seed and the
susceptibility of the host’s roots to infection. This in turn depends on the species of host
plant, age of root, size of root, water availability, age of seed, temperature and possibly
the nutritional status of the host plant.

• Damage to spikes by slugs, sheep and trampling as spikes emerge does occur, but this
may not be significant. Some of the flood-plain populations of O. reticulata may lose a
large proportion of the seed output in autumn floods.

• The burial of the seed in the soil at the correct depth for infection of the host plant is
vitally important and disturbance by rabbits, moles, livestock, man and floods may all
have an important role to play in this process. The presence of bare ground may be
important in this respect. Whether this enables the seeds of broomrapes to enter the soil
or whether it allows gaps for the establishment of young host plants or young roots of the
host plant to grow into is not clear.

Further gaps in our knowledge of the autecology of broomrapes which may be of

significance include the following:

• The species of pollinator and their distribution and abundance with respect to the
parasite.

• The ecological requirements of some of the host plants.

References

Allen, S. E., Grimshaw, H. M., Parkinson, J. A. and Quarmby, C. (1989). Chemical
Analysis of Ecological Materials. 2nd edition. Blackwell, Oxford.

Ashworth. L. J. (1976). Quantitative detection of seeds of branched broomrape in
California tomato soils. Plant Disease Reporter 60: 3 80-383.

BarNun, N. and Mayer, A. M. (1993). Preconditioning and germination of Orobanche
seeds: respiration and protein synthesis. Phytochemistry 34: 39-45.

Brown, R. (1946). Biological stimulation in germination. Nature 157: 64-68.

Brown, R., Greenwood, A. D., Johnson, A. W. and Long, A. G. (1951). The stimulant
involved in the germination of Orobanche minor Sm; I Assay technique and bulk
preparation of the stimulant. Biochemical Journal 48: 559.

Headley, A. D. and Jeavans, M. K. (1996). An investigation into the autecology of thistle
broomrape, Orobanche reticulata Wallr.: with special reference to seed germination,
seed banks and slug populations. Report to English Nature, York.

Headley, A. D. and Rumsey, F. J. (1998). The biology and ecology of Orobanche: a
bibliographic review. Naturalist 123: 89-98.

Hughes, M. (1995a). An investigation of the factors affecting the distribution of Orobanche
rapum-genistae and O. elatior in Britain. Undergraduate dissertation: University of
Bradford, Bradford.

Hughes, M. (1995b). An autecological study of Orobanche reticulata Wallr. in Yorkshire.
Report to English Nature, York. University of Bradford, Bradford.

Hughes, M. and Headley, A. D. (1996). The biology and ecology of the thistle broomrape,
Orobanche reticulata Wallr. Naturalist 121: 3-9.

Jeavans, M. K. (1996). The conservation of the thistle broomrape, Orobanche reticulata
Wallr. in Yorkshire. Undergraduate dissertation, University of Bradford.

Jones, M. (1989). Taxonomic and Ecological Studies on the Genus Orobanche L. in the
British Isles. Ph.D. thesis, University of Liverpool.

Kreutz, C. A. J. (1995). Orobanche. The European Broomrape Species. Vol. I: Central
Europe and Northern Europe. Stichting Natuur, Limburg.

Newlands, C. and Smith, H. (1998). The management of Orobanche reticulata Wallr.

70 Management and Conservation Status of Sites with Orobanche reticulata Populations

populations in Yorkshire, England. Naturalist 123: 70-75.

Pritchard, H. W. (1985). Determination of orchid seed viability using fluorescein diacetate.
Plant, Cell and Environment 8: 727-730.

Press, M .C. and Graves, J. D. (1995). Parasitic Plants. Chapman & Hall, London.
Salisbury, E. J. (1942). The Reproductive Capacity of Plants. Bell, London.

Sunderland, N. (1960). The production of the Striga and Orobanche germination
stimulants by maize roots; I. The number and variety of stimulants. Journal of
Experimental Botany 11: 236-245.

MANAGEMENT AND CONSERVATION STATUS OF SITES WITH
OROBANCHE RETICULATA WALLR. POPULATIONS

COLIN NEWLANDS

English Nature, Plumber to Pennines Team, Bullring House,

Northgate, Wakefield WE2 3BJ
AND

HELEN SMITH

English Nature, North and East Yorkshire Team, Genesis Building, Science Park,

Heslington, York YOl 5DQ

Introduction

English Nature's Species Action Plan for Orobanche reticulata Wallr. identifies the main
threats to the British populations as (a) destruction of the host plant primarily creeping
thistle ( Cirsium arvense); (b) loss of habitat through scrub invasion; and (c) loss to
competing land uses (Anon., 1996). The overall objective of the Action Plan is to
encourage sympathetic management of sites on which it occurs to maintain and increase
the population. The ecological requirements of O. reticulata are not yet fully understood,
and as a result, site management to benefit the species remains somewhat experimental.
The aim of the Plan so far has been to halt natural vegetation succession, for instance from
rough grassland to scrub, and create disturbed open ground to maintain stands of
C. arvense. Funding for some of this work has been through an English Nature Species
Recovery Programme grant.

A substantial proportion of the 27 separate extant British populations of O. reticulata fall
within the boundaries of various nature reserves or Sites of Special Scientific Interest
(SSSI) notified under the 1981 Wildlife and Countryside Act, as amended (Table 1). Of
these, only two. Cow Cliff pasture and quarry and Hook Moor, were notified specifically
on account of the presence of large populations of O. reticulata. The other SSSIs were
notified in order to conserve a range of habitats associated with the magnesian limestone or
riverine habitats. Nevertheless, maintaining the populations of O. reticulata on these sites
is a key consideration in site management. Additionally, the site at Ox Close Wood in West
Yorkshire is a nature reserve owned and managed by the East Keswick Wildlife Trust, and
identified as a Site of Ecological/Geological Interest in the Leeds City Council Unitary
Development Plan. The remaining 15 sites have no formal conservation status, although in
several cases the landowners take an interest in having O. reticulata on their land.
Therefore, for the majority of the individual populations the opportunity exists to undertake
positive management for the species, or influence broader site management to benefit O.
reticulata.

Naturalist 123 (1998)

Management and Conservation Status of Sites with Orobanche reticulata Populations 71

TABLE 1

The number of sites and proportion of the British population of O. reticulata with different
levels of conservation status. Effective population sizes are based on harmonic means of
the available population census data for all sites.

Conservation Status

No. of sites

British Population Size
Effective Size % of the total

Site of Special Scientific Interest
and nature reserve

3

9.4

2.9

Site of Scientific Interest and
private nature reserves

1

53.8

16.6

Site of Special Scientific Interest only

8

127.6

39.3

Without any conservation status

15

133.8

41.2

Developing Management Techniques

Developing management techniques to favour O. reticulata has focussed on six sites, Cow
Cliff pasture and quarry, Quarry Moor and Ripon Parks in North Yorkshire, and Hook
Moor, Hetchell Wood and Ox Close Wood in West Yorkshire. All provide important
opportunities to study the effects of different techniques on O. reticulata populations. At
Hook Moor and Cow Cliff pasture and quarry, where the only significant claim to
conservation status is the presence of O. reticulata, this does not conflict with other site
objectives. At the others, maintaining O. reticulata is only one of a number of nature
conservation objectives. Given that the primary host of O. reticulata is C. arvense, a
notifiable agricultural weed species, it is clear that there can be a conflict of interest with
other grassland management and restoration objectives. Management practices carried out
on the above six sites in recent years are listed in Table 2.

TABLE 2

Management on six sites with populations of Orobanche reticulata.

Site

Management

Cow Cliff pasture and quarry SSSI

Scrub removal/rotovation of ground

Quarry Moor SSSI

Scrub removal/cattle and sheep grazing/scraping
off topsoil

Ripon Parks SSSI

Scrub removal/sheep and goat grazing

Hook Moor SSSI

Scrub removal/soil ripping

Hetchell Wood SSSI

Mowing/grazing

Ox Close Wood

Mowing/coppicing/clear cutting/grazing

A number of sites on which O. reticulata occurs have little or no management. Many are
not grazed by domestic stock, and are prone to scrub encroachment. Succession from
grassland to dense scrub results in the decline and eventual loss of the host plant. Scrub
control was undertaken at Hook Moor, where hawthorn ( Crataegus monogyna ) and gorse
( Ulex europaeus) had colonised the road embankments. At this site bramble ( Rubus
fruticosus agg.), dog rose ( Rosa canina) and nettle ( Urtica dioica) were also cut back, as
monitoring of O. reticulata showed that these species, growing unchecked, formed dense
stands which out-competed C. an’ense. It has been noted, however, that O. reticulata does
sometimes parasitise thistles growing under shrubs in rough grass (Hughes, 1996), and
amongst scattered bushes of Crataegus where the plant tends to occur on thistles on the
sheltered, sunny side of the shrub (Abbott, 1996). It has not been recorded growing where
the shrub canopy is closed (Abbott, 1996). On this basis, scrub control need not necessarily

72 Management and Conservation Status of Sites with Orobanche reticulata Populations

aim at total eradication to benefit 0. reticulata.

In managing sites with 0. reticulata populations it has become evident that ground
disturbance is a very important factor. At Ox Close Wood, dead flower spikes of the plant
were first noticed in 1992. It is assumed that the species first appeared in 1991, two years
after a section of the wood was clear-felled. It is likely that seed was already present in the
soil, and the growth of the thistles which colonised the open, disturbed ground in the clear-
fell provided the opportunity for it to germinate. The same happened at Hetchell Wood,
where the plant appeared in an area coppiced by the Yorkshire Wildlife Trust two years
previously. This new site was only a short distance south of the limestone grassland within
the woodland where the species has been recorded for many years. Ground disturbance by
soil ripping and light rotovation has taken place on some sites, most notably at Cow Cliff
pasture where O. reticulata showed a large increase in numbers two years after rotovation
and a consequent expansion of C. arvense.

Where populations of O. reticulata occur on sites grazed by domestic stock, such as
Ripon Parks, there can be a conflict of interest as stated above. The species-rich grassland
is a key reason for Ripon Parks being designated a SSSI and the extensive thistle
encroachment is of concern from both a nature conservation and a stock management point
of view. Observations from Ripon Parks and Hetchell Wood have confirmed that
O. reticulata does not do well where the C. arvense stands become very dense (Hughes &
Headley, 1996). On these grazed grassland sites, a compromise is reached by controlling
the thistles to the extent of leaving only small groups or scattered individuals which will
not adversely affect the broad management objectives of the site, yet will retain the
O. reticulata population. It should be noted, however, that sheep at Ripon Parks, and
livestock on other sites, have been reported to graze young spikes of O. reticulata (Hughes,
1996), although at current levels this is not felt to be a threat to the survival of the
population within the SSSI.

In order to investigate the effects of different management techniques, in 1994 a project
was set up under the Species Recovery Plan at Ox Close Wood. Five 25 x 25m plots were
established in the felled area of the wood where O. reticulata had appeared three years
previously. Each received a different type of management as follows: (a) mowing the field
layer and leaving the woody regrowth, (b) coppicing all trees on a 5-year rotation, (c)
grazing with goats, (d) clear-cutting of all vegetation and (e) a control plot with no
management.

Response of O. reticulata to Management

Monitoring of the O. reticulata populations has shown that the number of flowering spikes
present at each of the sites can be prone to dramatic annual fluctuations (Headley et al .,
1998a). However, the overall population across the suite of sites remains comparable
(Abbott, 1996, 1997). Trying to equate management effects directly to population trends
within a site is problematical, since no consistent pattern emerges over time. Hook Moor
and Ox Close Wood serve as examples.

Table 3 shows the type of management that has taken place at Hook Moor, together with
the numbers of O. reticulata spikes. In 1995 there was an increase in numbers in all four
quadrants, although only one was managed. However, 1995 was a good year for the
species, with annual monitoring showing increases at many sites. Continuously hot weather
during the summer is likely to have been a contributing factor to this general increase in
Dowering. Scrub control and other work was carried out in October. The counts for 1996
showed a dramatic increase in O. reticulata numbers in two quadrants where management
was undertaken. The area cleared of scrub had however suffered a reduction in numbers, as
did the quadrant treated in 1994. In the north-west quadrant it was noted that rabbits were
prolific on the road embankment. It is likely that rabbits play an important role at Hook
Moor in maintaining open, disturbed ground after scrub clearance. This may well aid the
burying of O. reticulata seed (Headley et al., 1998b), and certainly creates suitable
conditions for the establishment of C. arvense.

TABLE 3

Numbers of Orobanche reticulata flower spikes (numbers in bold) and management activities at
Hook Moor Site of Special Scientific Interest in the years from 1991 to 1997.

Management and Conservation Status of Sites with Orobanche reticulata Populations 73

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74 Management and Conservation Status of Sites with Orobanche reticulata Populations

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Changes in numbers of flowering spikes of Orobanche reticulata between 1994 and 1997
in separate plots treated in different ways at Ox Close Wood nature reserve.

The benefit of rabbit grazing and burrowing after management work can be shown by
contrasting Hook Moor with Hetchell Wood. At Hetchell Wood numbers of O. reticulata
in the coppice plot described above fell sharply between the counts of 1994 and 1995,
probably due to the very dense regrowth of tall herbs, including C. arvense , as well as the
coppice stools during 1995. With no control of the vegetation by large herbivores, there
was little bare ground present for thistle seedling establishment.

After its first appearance in 1991, 1995 was a very productive year for O. reticulata at
Ox Close Wood (Fig. 1). All but one plot showed an increase in flowering spikes. Large
increases were noted in the plot mown in February with the woody growth left (herbcut),
and in the plot clear-cut in February. Elsewhere in the wood. 59 spikes appeared where
new steps had been created two years previously, and 67 spikes appeared for the first time
in a new enclosure grazed by goats. By contrast, in 1996 there was a dramatic fall in
numbers throughout the wood which has continued into 1997, including the experimental
plots (Fig. I). Even in the plot which had been clearcut in February and again in November
1995, the number of O. reticulata spikes has fallen markedly (Fig. 1). The reason for this
decrease is almost certainly the unchecked rapid expansion of Rubus and bracken
(Pteridium aquilinum ) in the years following clear-felling, which had a suppressive effect
upon C. arvense and reduced the area of bare soil available for seedlings of C. arvense to

Management and Conservation Status of Sites with Orobanche reticulata Populations 75

establish in. Even in the goat-grazed enclosures it would appear that the goats did not
significantly affect the vigorous growth of Rubus. As at Hetchell Wood, the contribution of
wild grazers to maintaining areas of open, disturbed ground was not significant.

Conclusions

The following conclusions are to be drawn from the management experience gained to date
from those sites where O. reticulata has responded to habitat management, either planned
or coincidental, and has been subject to population monitoring:

• Ground disturbance is beneficial for both the host plant and O. reticulata.

• O. reticulata appears in the second or third year following disturbance of the ground.

The following recommendations can also be made with regard to managing sites for O.
reticulata:

• Moderate numbers of rabbits should be encouraged in order to create bare patches for
thistles to colonise and aid burial of O. reticulata seed.

• An open sward should be maintained to provide opportunities for thistles to colonise.

• Ideally scrub control should be carried out mechanically rather than chemically as the
disturbance of the ground after O. reticulata plants have set seed may be beneficial.

• Dense stands of Rubus fruticosus and other vigorous tall herbs and woody perennials,
which invade open areas and out-compete thistles, need to be controlled.

• Vegetation management should not be undertaken between the very beginning of
flowering (early June) and the completion of seed set (end of September/early October).

References

Abbott, P. P. (1991, unpubl.). Orobanche reticulata in West Yorkshire. English Nature,
Wakefield.

Abbott, P. P. (1994, unpubl.). Orobanche reticulata in West Yorkshire. English Nature,
Wakefield.

Abbott, P. P. (1995, unpubl.). Orobanche reticulata in Yorkshire. Leeds City Council,
Leeds.

Abbott, P. P. (1996, unpubl.). Orobanche reticulata in Yorkshire. Leeds City Council,
Leeds.

Abbott, P. P. (1997, unpubl.). Orobanche reticulata in Yorkshire. Leeds City Council,
Leeds.

Anon. (1996). Thistle Broomrape Orobanche reticulate Species Action Plan. English
Nature, Peterborough.

Headley, A. D., Abbott, P. P. and Foley, M. (1998a). Monitoring of Orobanche reticulata
Wallr. populations in Yorkshire, England. Naturalist 123: 56-60.

Headley, A. D., Hughes, M. and Jeavans, M. K. (1998b). Autecological studies on
Orobanche reticulata Wallr. and the implications for management. Naturalist 123: 60-
70.

Hughes, M. (1996). An autecological study of Orobanche reticulata Wallr. in Yorkshire.

Report to English Nature, York. University of Bradford, Bradford.

Hughes, M. and Headley, A. D. (1996). The biology and ecology of the thistle broomrape,
Orobanche reticulata Wallr. Naturalist 121: 3-10.

76

ARE BRITISH OROBANCHE SPECIES IN DECLINE?

FRED RUMSEY

Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD

AND

ALISTAIR HEADLEY

Department of Environmental Science, University of Bradford, Bradford BD7 IDP
Introduction

The necessity for monitoring rare and vulnerable species is now widely acknowledged. As
conservation becomes pro-active, for example Plantlife’s ‘Back from the Brink’ scheme and
the developing suite of recovery programmes initiated under the Biodiversity Action Plan
(Anon., 1995), it is becoming more important to audit what may be very costly proposed
actions. Information on the autecology, reproductive biology and numbers is required to
assess the suitability of such programmes and judgements on the risks involved. Many
annual or monocarpic species show marked fluctuations in population size. Orobanche
species, present at their northern extremes of range, are reliant on suitable, and perhaps
exceptional climatic conditions to grow and reproduce successfully. They must also rely on
the abundance and vigour of populations of their host plants.

It is therefore not surprising that this genus is well known for extreme annual variance in
numbers. To what extent then do we need to study the distribution not just of one species,
but two or more? The necessity for the close presence of a host to elicit germination would
suggest that to some extent abundance of parasite and host must be linked. However, none
of our broomrape species are uniformly distributed throughout the ranges of their host(s).
The observations by Headley et al. (1998) and others also indicate that while it is a
necessity that host plants are abundant for parasite numbers to be high, parasite numbers are
not solely dictated by host abundance.

In addition to obvious climatic and edaphic conditions acting at the broad geographic
level, many factors may be acting to limit parasite numbers within ‘suitable’ areas. These
factors may include predation from other species; for example pre-emergence grazing by
slugs, or perhaps more significantly, temporal changes in host susceptibility linked to the
age structure of the host population. The latter might be expected to have a more profound
effect on annual Orobanche species than perennial, as the latter can persist on/in a host root
system and are not reliant on a suitable novel root presence for germination each year. It is
unclear as to which British species of broomrape can perennate, although it is probable that
only O. rapum-genistae, and to a lesser extent O. elatior, are perennial over several years. It
is these species that occur in more stable communities, where disturbance and recruitment
of new hosts is generally at a lower level than in the ruderal, cliff edge and dune
communities favoured by the annual species. None of the species occur in climax
communities and all will be reliant on disturbance, albeit less regular for perennials, to
maintain flowering populations.

The apparent ability of Orobanche species to form a persistent seed bank enables them to
exploit patchy environments that recur cyclically over time. Any species which is
potentially highly dispersible and reliant on a patchy unstable environment might be
expected to come and go. This means that they are apparently losing and gaining sites all
the time due to the presence of a persistent seed bank, which therefore makes it difficult to
prove extinction at a specific site. The fluctuation in population size, apparent absences and
production of ephemeral populations pose problems when determining whether the species
numbers overall are significantly changing over time. This is important for making
decisions as to whether a species is in decline or not. Such information can only realistically
be deduced if we have an accurate idea of the distribution and population sizes of the
species over time.

Our knowledge of the true distribution of all taxa is reliant upon the level of recording
activity and the expertise of those recording (Rich & Woodruff, 1992). ‘Unusual’ plants and

Naturalist 123(1998)

77

Are British Orobanche species in decline?

those known to be rare, such as the broomrapes, attract attention and therefore might be
expected to be more regularly noticed and recorded than many plant genera. However, the
difficulty in accurately discriminating between taxa will result in a higher than average
proportion of dubious records in this genus. This is a particular problem if spurious records
inflate locality numbers and thereby influence decisions on legal protection, Action plant
listing, etc.

Much of our knowledge of the distribution of British plants comes from national atlases
of plant distribution as well as local floras (Perring et al ., 1962, 1976; Stewart et al. , 1994).
The use of maps in national atlases recorded on a hectad basis (10km x 10km grid squares)
or recent local floras at 5km or tetrad basis (2km) can be criticised, regardless of scale, if
they are used alone in assessing abundance. They do not give a true picture of the dynamics
of the species' occurrence; for instance, it is impossible to discriminate between a situation
where a species may be constantly dominant over an area of several kilometres or present as
single individuals at a few sites over a protracted period. The latter will give rise to a greater
proportion of dots on a map for the same number of individuals of a species than the former.
The Orobanche species tend to occur as small and sometimes ephemeral populations and
therefore fit the latter category. They will always in a sense be over-represented by a dot
mapping scheme. We must also consider that the number of records of such unpredictable
species is likely to be more a function of the effort put into recording them than their
absolute frequency.

Given these provisos we must start somewhere in identifying changing patterns in
distribution and overall scarcity and the published hectad maps give us a snapshot of change
over the last century. The numerous local and county floras provide an additional source of
information with, in many cases, a subjective quantification. These publications vary greatly
in style and content, making comparisons between and within areas and with earlier
accounts difficult. They are thus of limited use, but provide supplementary information to
mapped distribution data. From these it is possible to infer much as to the status and
distribution of a species over time and thus determine those taxa needing further scrutiny.

Using the data in Perring et al. (1962), Rumsey and Jury (1991), Stewart et al. (1994) and
subsequent records published in Watsonia, maps for a range of the rarer British species of
Orobanche have been produced (Figs. 1, 2, 3, 5 and 6). New hectad records made after 1970
are indicated by arrows and give an impression of the flux. In all cases the frequency of
occupied hectads has declined by 50% or more for those species examined here. In the case
of O. picridis and O. rapum-genistae this decline is apparently 80% or more.

Orobanche caryophyllacea (Fig. 1)

In spite of an abundance of suitable hosts this species has apparently never expanded
beyond its limited range on the Kent coast. Records from Argyll and N. Wales are
considered to be errors through accidental or deliberate mixing of herbarium specimens
(Rumsey, 1985). Records from Suffolk are supported by specimens and require
confirmation. The limited British range cannot be ascribed solely to climatic factors as the
species is thriving where introduced at Kew (Milne-Redhead, 1985). The most recent
published account of the species’ status is that in Philp’s (1982) atlas and thus its current
status is unclear. The loss of outlying populations following increased urbanization and
agricultural change may have restricted it to two hectads. There is no regular monitoring
and it appears the number of populations in Kent, let alone their size, is not known.
However, in good years the population at Sandwich can be more than 100 spikes. The
survey of past sites and monitoring of population size in the few remaining known sites
should be considered a priority.

Orobanche picridis (Fig. 2)

In terms of currently occupied hectads versus past records this species has apparently shown
the greatest proportional decline; however, several factors must be taken into consideration
before concluding that this species is necessarily the most threatened. The past confusion of

78

Are British Orobanche species in decline?

FIGURE 1

The distribution of Orobanche caryophyllacea records in Britain before 1970
(small circles) and from 1990 onwards (large circles). A cross represents an introduction.

this species with O. minor may have inflated the number of historical records, not all of
which are supported by specimens. As with O. minor, it is probable that past introductions
of O. picridis with crop seed may have produced additional, but ephemeral populations.
Two post- 1950 records relate to single or few individuals at sites in only one year. A better
picture of the species’ conservation status or ‘health’ can be gauged by studying its core
populations. Of these, only that in the Haslingfield and Comberton area of Cambridgeshire
has been lost. The fact that the three other known populations have persisted for over a
century is encouraging. However, population sizes are regularly in single figures and the

Are British Orobanche species in decline?

79

The distribution of Orobanche picridis (syn. O. artemisiae-campestris) records in Britain
before 1950 (open circles), 1950 to 1990 (small filled circles) and from 1990 onwards
(large filled circles). Arrows indicate new records after 1970.

species is reliant on a particular habitat on coastal chalk cliff ledges where the whole
population and seed bank could potentially fall into the English Channel. A recent search of
an area of chalk downland at the smaller of its two extant populations in Kent revealed a
total of 36 spikes. This population has been small throughout the 1980s. There is no
monitoring of the population on the Isle of Wight, due in part to being half-way up a 100m
chalk cliff on a ledge. The presence of the plant on the cliff ledges is occasionally noted
with the use of binoculars. Although an on-going programme of monitoring is desirable,
there are clearly practical problems in carrying this out. Further action such as establishment

80 Are British Orobanche species in decline?

of ex situ populations should be considered, given the precarious nature of the extant
populations.

Orobanche rapum-genistae (Fig. 3)

Undoubtedly this species has declined the most in terms of the absolute number of sites and
contraction in range. The most commonly encountered Orobanche in the early 19th century
is now a considerable rarity. The bleak picture of progressive decline presented in Stewart et
al. (1994) masks the true situation. If hectad records are treated as date classes, i.e. presence

The distribution of Orobanche rapum-genistae records in Britain before 1930 (open circles),
between 1950 and 1970 (small filled circles) and after 1970 (large filled circles). Arrows

indicate new records after 1970.

Are British Orobanche species in decline?

81

300

250

O

150

X)

§ 100 -

z

50 -

0

pre 1930

1930-

1950

1950-

1970

1970-

1980

1980

onwards

FIGURE 4

The number of hectads in which Orobanche rapum-genistae has occurred in Britain over
different time intervals (taken from Hughes, 1995).

is not inflated by earlier or later records, we see that currently numbers appear to be higher
than in the period 1930-1950 and they have remained at a similar level since concerted
recording began in the 1950s (Fig. 4). The lower figure for 1930-1950, as taken from the
1962 atlas, may be a reflection of lower recording activity during this period. It is clear that
the major decline in this species occurred much earlier with the wide-scale changes in land
use during the last century and early part of this century. The creation of numerous and wide
road verges, especially on the motorway system, has provided a novel and suitable habitat
for large populations of its host plants, gorse and broom. This factor and the run of hot
summers in the 1970s may be responsible for the small rise in records in the 1970s and

Can we therefore afford to be complacent about the conservation of this species? In an
attempt to assess the abundance of this species in the hectads from which it is reported and
whether these populations are persisting, accounts from a range of county floras covering
the past English distribution are briefly summarised in Table 1. Where possible the number
of reported sites is given. Unfortunately, earlier accounts are often poorly localised, or
single sites may be listed under many names depending on the individual recorder. Many
recent floras give the number of tetrads/hectads, etc, but they give no indication of the
number of populations or sites within them. The figures presented must therefore be treated
with some caution. What is clear is that hectad numbers do not differ markedly from site
numbers, i.e. each ‘dot’ on a distribution map represents a single population in most cases.
Many of these records are of single individuals, with few populations producing larger
numbers, i.e. >20 spikes or clumps. In those areas in which the species is most frequent, for
example in south-west England and Wales, although the total number of populations has
remained relatively constant, there is some flux in the populations. Population losses are
therefore currently balanced by the appearance of new populations. The factors affecting the
persistence of this species should be investigated. The potential to recover ‘lost’ sites from
seed banks is evident from the return of the species when woodland stands reverted to heath
scrub after the great storm of 1987.

Many potentially suitable areas of gorse and broom scrub now exist, but effective
management to open these stands and encourage recruitment would undoubtedly be
beneficial. This striking species may still be somewhat under-recorded as stands of its main
hosts are unpleasant areas to investigate.

1980s.

82

Are British Orobanche species in decline?

TABLE I

Number of reported sites of Orobanche rapum-genistae in different counties of England and

Wales.

County

Before 1950

1950-1980

After 1980

Bedfordshire

absent

absent

absent

Berkshire

4

absent

absent

Buckinghamshire

6

1

absent

Cambridgeshire

3

absent

absent

Cornwall

20

4

4

Cumbria

c. 14

4

2

Devon

34

1 1

7

Dorset

1 1

2?

7

Durham

7

absent

absent

Essex

15

1

absent

Glamorgan

10

absent

absent

Gloucestershire

14

absent

absent

Hampshire

29

10

6

Hertfordshire

c. 14

1

absent

Kent

c. 20

>8

7

Lincolnshire

1

1

1

Middlesex

2

absent

absent

Norfolk

1 1

absent

1?

Northumberland

>22

?

6

Oxfordshire

absent

absent

absent

Somerset

6

3

7

Suffolk

c. 15

7

1?

Surrey

9

1

1

Sussex

41

7

6?

Wiltshire

21

absent

absent

Orobanche minor var. maritima (Fig. 5)

Since this taxon has been the subject of considerable taxonomic and nomenclatural
confusion, the map is therefore unlikely to be entirely accurate. As the habitat occupied by
this species has not been significantly affected by land-use changes over the last century, it
is probable that the decline of this species is apparent rather than real. Massive population
fluctuations have been reported from various parts of its range, e.g. the Isle of Wight
(Shepherd, 1983) and Jersey (Le Sueur, 1984). Although this taxon is not endemic, it is
more frequent in the British Isles than elsewhere. This feature sets it apart from all the other
species considered here, all of which must be considered not to be threatened on a global
scale. Its true extent and in particular its continued survival in the somewhat isolated Kent
populations, where it grows with O. picridis , requires investigation.

Orobanche purpurea (Fig. 6)

Like O. minor var. maritima, this is primarily a maritime species. However, it is not found
exclusively in these areas, with recent finds almost as likely to come from inland pastures
and churchyards than from coastal locations. Unlike the other species considered here, a
high proportion of the hectad occurrences of this species refer to recent expansions in range.
If this species becomes established in these new sites, as it seems to have done at Maryport
in Cumbria, this may influence its conservation status. There has been some monitoring of
the size of the population at Maryport and its only known extant population in Wales (Fig.
7). Again, this species of Orobanche shows marked fluctuations in population size. In 1994

Are British Orobanche species in decline?

83

FIGURE 5

The distribution of Orobanche minor war. maritima (syn. 0. maritima ) records in Britain
before 1950 (open circles), between 1950 and 1970 (small filled circles) and after 1970
(large filled circles). Question marks indicate doubtful records.

and 1995 spikes were reported to be present by the original discoverer of this population,
but despite there being few spikes, they were not counted. A formalised programme of
monitoring of these novel sites should be considered. The abundance of this species’ host,
Achillea millefolium , would indicate that either poor dispersal or particular climatic and
edaphic factors are limiting the parasite’s range. It could prove an interesting experimental
organism upon which to study these questions.

84

Are British Orobanche species in decline?

FIGURE 6

The distribution of Orobanche purpurea in Britain before 1950 (open circles), between
1950 and 1980 (small closed circles) and after 1980 (large closed circles).

Why is monitoring necessary?

As yet we have little understanding of many aspects of the ecology and biology of these
unusual organisms. In the absence of extensive laboratory studies, an organised programme
of field observation and recording will, over time, provide relevant information useful for
determining conservation actions. To date, only 0. reticulata can be said to have been the
subject of any concerted censusing of population size. Even with this species we as yet have
too little data to decide whether it is stable, or undergoing a protracted but inexorable
decline.

Are British Orobanche species in decline?

85

Year

FIGURE 7

The inter-annual variations in the size (number of flowering spikes) of the Orobanche
purpurea population in Pembrokeshire. Data kindly provided by A. Jones.

Acknowledgements

We wish to express our gratitude to Andy Jones of the Countryside Council for Wales for

providing the census data of the Orobanche purpurea population in Pembrokeshire.

References

Anon. (1995). Biodiversity: the UK steering group report, Volume 2: Action plans. HMSO,
London.

Headley, A. D., Abbott, P. P. and Foley, M. (1998a). Monitoring of Orobanche reticulata
Wallr. populations in Yorkshire, England. Naturalist 123: 56-60..

Hughes, M. (1995). An investigation of the factors affecting the distribution of Orobanche
rapum-genistae and O. elatior in Britain. Undergraduate dissertation: University of
Bradford, Bradford.

Le Sueur, F. (1984). Flora of Jersey. Societe Jersiaise, St Helier.

Milne-Redhead, E. (1985). More hosts of Orobanche. B.S.B.I. News 41, 29.

Perring, F. H. and Walters, S. M. (1962). Atlas of the British Flora. Cambridge University
Press, Cambridge.

Perring, F. H. and Walters, S. M. (1976). Atlas of the British Flora. 2nd ed. Cambridge
University Press, Cambridge.

Philp, E. G. (1982). Atlas of the Flora of Kent. Kent Field Club. Maidstone.

Pickering, A. T. ( 1 992). Growing Orobanche purpurea Jacq. from seed. Watsonia 19: p. 1 8.

Rich, T. C. G. and Woodruff, E. R. (1992). The influence of recording bias in botanical
surveys: examples from the B.S.B.I. monitoring scheme 1987-1988. Watsonia 19: 73-95.

Rumsey, F. J. (1985). Orobanche caryophyllacea Sm. in N. Wales? Watsonia 15: 277 .

Rumsey, F. J. and Jury, S. L. (1991). An account of Orobanche L. in Britain and Ireland.
Watsonia 18, 257-295.

Shephard, B. (1983). Supplement to the Flora of the Isle of Wight. Newport.

Stewart, A., Pearman, D. A. and Preston, C. D. (1994). Scarce plants in Britain. English
Nature, Peterborough.

86

THE WAY FORWARD FOR BROOMRAPE
CONSERVATION IN BRITAIN

ALISTAIR D. HEADLEY

Department of Environmental Science, University of Bradford, Bradford BD7 l DP

FRED J. RUMSEY

Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD

AND

IAN TAYLOR

English Nature, Manor Barn, Over Haddon, Bakewell, Derbyshire DE45 1EJ

Nearly all the rarer species of broomrape (O. artemisiae-campestris, O. caryophyllacea, O.
reticulata, O. purpurea and O. rapum-genistae) present the same problems for their
conservation. Firstly, most of them have very common host plants, such as Achillea
millefolium, Cirsium arvense, Cytisus scoparius. Thymus praecox, Galium mollugo, G.
verum and Ulex europaeus , or hosts that are at least locally abundant, such as Picris
hieracioides (Rumsey & Jury, 1991). Secondly, they occur in relatively common, or at
least not rare, habitats and often unattractive sites and are therefore not rated highly by
conservation bodies. If anything, the broomrapes frequently occur in weedy and
uninspiring grasslands or waste places, for example Maryport docks and the embankments
of major roads. Some occur in inaccessible locations, such as chalk seacliffs, or in
uncomfortable vegetation, such as gorse thickets and stands of thistles and nettles. If some
of the sites had not been designated as SSSIs for the broomrapes themselves, it would have
meant that the broomrapes would have largely slipped through the system of habitat
protection or association with other rare organisms.

The large inter-annual fluctuations in numbers also count against them in terms of
identifying controlling factors governing population size. The timing of flowering is also
very variable between years for many species and therefore makes it more difficult to make
a census of the populations. It is clear that there is very little systematic monitoring of
populations for all species except O. reticulata (Rumsey & Headley, 1998a). The status
and size of the British populations of Orobanche is therefore largely unknown (Rumsey &
Headley, 1998a). There is consequently a very poor understanding of the factors that
govern population size and the size of the host populations do not always appear to be the
most important factor in determining the size of the parasite population.

Some understanding has been gained of the management requirements for O. reticulata,
but different species of host will almost certainly have their own specific requirements.
Despite this, the different species of Orobanche are likely to have some requirements in
common as they possess the same parasitic life-cycle.

It is clear that most rare species of broomrape in Britain suffer from the same problems
of (i) lack of monitoring of the number and size of populations, (ii) poor understanding of
their ecology, (iii) a currently low profile in the Biodiversity Action Plans and (iv) a
complex parasitic life-cycle. It is extraordinary that a genus which has such a large
proportion of its species (7 out of a total of 9) in the Red Data, Near Threatened or
Nationally Scarce categories has been largely overlooked in terms of its conservation.

Achievements to date

The workshop has certainly helped the conservation of broomrapes in the UK at least. A
network of people working on the biology, conservation and management of sites with rare
species of Orobanche has been established. This will enable conservationists and managers
to obtain advice on management problems with greater ease. The workshop has passed on
many of Ihe lessons learnt from conserving and researching O. reticulata to those with
responsibilities for conserving other rare species of Orobanche. The Thistle Broomrape
Newsletter has succeeded in increasing awareness of this plant. Despite some inaccuracies

Naturalist 123 ( 1998)

The Way Forward for Broomrape Conservation in Britain 87

in articles in the local and national press, the publicity surrounding this species can only be

to the benefit of conservation organisations.

Issues

The following are issues raised at the workshop which are relevant and important in the

conservation of Orobanche in general as well as being specific to O. reticulata.

• It is not clear which nomenclature should be followed with regard to O. reticulata. It may
be either O. reticulata sensu stricta or (). pallidiflora or 0. reticulata ssp. procera. This
needs to be resolved by carrying out genetic studies of the British material alongside
European material of the two species described by Kreutz (1995). This same issue also
applies to the various subspecies of O. minor, some of which are regarded by some
workers as worthy of specific rank (Rumsey, 1998). This has important implications for
their status and conservation.

• The assertion that there may be significant inbreeding and consequent erosion and loss of
genetic variation in the small populations of O. reticulata, as suggested by Headley et al.
(1998b), needs to be checked. The population studies may also suggest that there are
perhaps fewer effective populations of O. reticulata in Yorkshire than might be initially
apparent due to seed dispersal along rivers from larger donor populations to smaller non-
viable recipient populations (Headley et al., 1998a).

■ • The monitoring of the number and size of the extant populations of the three most
threatened species of Orobanche in Britain, O. artemisiae-campestris, O. caryophyllacea
and O. purpurea, is lacking and needs remedying. This requires urgent attention to
ascertain if populations are on the decline. A ten-year period of monitoring should give
an indication of any significant trend in population size.

Actions

• Establish working groups. An informal network of people working on the biology,
conservation and management of sites with rare species of broomrape now exists and Dr
Headley is willing to act as co-ordinator.

• Publicise and disseminate information. These proceedings are intended to disseminate
the current state of knowledge to managers, conservation officers and researchers and
will help others make better informed judgements in managing and conserving these
species or sites where they exist. There is the intention to broaden the Thistle Broomrape
Newsletter to cover the whole genus. This will increase the readership in number and
geographical spread in the U.K.

• Establish effective monitoring. Monitoring of population sizes of priority species should
be initiated as soon as possible. It is recommended that all extant populations of O.
artemisiae-campestris and O. caryophyllacea be monitored and for O. reticulata that the
largest sites and those with a history of recording of at least 4 previous years, be carried
out. O. purpurea also appears to require some monitoring, preferably at all extant sites.
The decline in O. rapum-genistae needs confirming by the monitoring of a number of
sites with known management scattered throughout the U.K. The co-ordination of
recording could be carried out by a single person or organisation, but the actual
monitoring could be carried out by the local and most appropriate organisations with the
populations of broomrape in their areas. The abundance and vigour of the host plants in
the sites where the species of Orobanche occur should also be monitored in some way.

• Species Action Plans. Ideally, these need to be prepared for O. artemisiae-campestris, O.
caryophyllacea and O. purpurea. It was felt, however, that there was little to be gained
from trying to press for raising O. artemisiae campestris, O. caryophyllacea and O.
reticulata from the ‘long’ to the ‘middle’ list of the Biodiversity Action Plan, but their
inclusion in local action plans should be encouraged. The local Biodiversity Action Plan

88

The Way Forward for Broomrape Conservation in Britain

for Kent has been produced, yet neither 0. caryophyllacea , restricted to this county, or 0.
artemisiae-campestris, with two of its three extant populations, have been considered as
species worthy of action!

• Old Sites. Former localities of broomrape should be surveyed for the presence of the host
plant/s as well as the Orobanche , current land-use, vegetation and suitability for re-
establishment of populations. If felt appropriate or worthwhile, soil samples could be
collected to establish the continuing presence of a seed bank at those sites suitable for
population re-establishment. Soil samples could be processed at one laboratory. All
former sites of O. artemisiae-campestris, O. caryophyllacea and O. purpurea
populations should be examined.

• Life span. There are many aspects of the autecology of Orobanche that are poorly
understood. The length of the life-cycle in all the native Orobanche needs to be
determined by cultivating plants on host plants in appropriate experimental conditions.
The life-cycle in O. reticulata is likely to be monocarpic and usually completed within a
year, but those of O. rapum-genistae and O. elatior may be polycarpic and perennial.

• Soil/host nutrient status. The influence of soil or host nutrient status on susceptibility to
infection requires investigation. This is important in order to establish whether nutrient
enrichment of the soil poses a significant rather than an imagined threat to any
Orobanche population.

• Host-parasite relationships. A sound knowledge of the ecology and population dynamics
of the host plants is also vital to the conservation of the Orobanche in question. Many of
the host plants are very common, but our understanding of their autecology is not as
complete as one would like.

• Ex-situ cultivation and propagation. Considering the precarious position and nature of
the extant populations of O. artemisiae-campestris (Rumsey, 1998) they will require the
re-establishment of extinct populations or establishment of a population in a suitably safe
locality. Ex-situ cultivation will provide a safety net for those populations that may be
lost due to natural catastrophic events such as collapse of cliff ledges (e.g. O. artemisiae-
campestris) or floods (e.g. O. reticulata), or developments, such as road-widening and
flood defences (e.g. O. reticulata). This can also form the basis for the re-establishment
of extinct populations or to establish ‘safe’ populations elsewhere. The ex-situ
cultivation and propagation of the rarer Orobanche will therefore be necessary to bulk-
up seed for any re-establishment of extinct populations.

• Seed Viability. The development of effective means of ex-situ methods of propagation of
plants from seed is also required by workers at the Millenium Seed Bank at Kew in order
to replace collections of seed that have lost their germinability or viability. In this regard,
the optimum storage conditions for seeds needs to be investigated and more rigorous
checks on whether current storage conditions at Wakehurst Place are the best for these
seeds. These matters will be raised with the newly appointed staff member responsible
for microscopic seeded species. This applies to all of the rare and threatened species of
broomrape.

• Svstematics and breeding systems - a molecular approach. The taxonomic status of O.
reticulata, O. artemisiae-campestris and subspecies of O. minor need to be elucidated
with the latest molecular techniques. The British material of the rarer species of
Orobanche may be genetically depauperate and/or genetically distinct from mainland
European populations. Therefore the degree of genetic variation in the rare species of
broomrape in Britain and its similarity to Continental European material requires urgent
investigation. This will also help to shed light on whether the low population densities
and vigour of some of the populations or species is due to inbreeding depression.

89

The Biology and Ecology 0/ Orobanche: a Bibliographic Review

Despite the rapid progress in understanding the ecology of O. reticulata , there is still
much that is not known about the ecology and conservation of nearly all of the species of
Orobanche in Britain. If nothing is done to rectify this situation we may see at least one
species of Orobanche become extinct in the British Isles soon, or more become even rarer.

References

Headley, A. D., Abbott, P. P. and Foley, M. (1998a). Monitoring of Orobanche reticulata
Wallr. populations in Yorkshire, England. Naturalist 123: 56-60.

Headley, A. D., Hughes, M. and Jeavans, M. K. (1998b). Some aspects of the autecology
of Orobanche reticulata Wallr. and the implications for management. Naturalist
123: 60-70.

Kreutz, C. A. J. (1995). Orobanche. The European Broomrape Species. Vol. 1: Central
Europe and Northern Europe. Stichting Natuur, Limburg.

Newlands, C. and Smith, H. (1998). Management and conservation status of sites with
Orobanche reticulata Wallr. populations. Naturalist 123: 70-75.

Rumsey, F. J. (1998). Taxonomic problems in the Orobanchaceae - the British
perspective. Naturalist 123: 50-53.

Rumsey, F. J. and Headley, A. D. (1998). Are British Orobanche species in decline?
Naturalist 123: 76-85.

Rumsey, F. J. and Jury, S. L. (1991). An account of Orobanche L. in Britain and Ireland.
Watsonia 18: 257-295.

THE BIOLOGY AND ECOLOGY OF OROBANCHE:

A BIBLIOGRAPHIC REVIEW

ALISTAIR D. HEADLEY

Department of Environmental Science, University of Bradford, Bradford BD IDE

AND

FRED J. RUMSEY

Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD

Although it is not possible in a limited space to give a comprehensive review of the biology
and ecology of species of broomrape other than O. reticulata , it is hoped that this paper
will give a fair reflection of knowledge on the genus as a whole. It does serve to highlight
the paucity of information relating to most non-crop weed species, which includes those
species of Orobanche found in the British Isles.

The broomrapes are root holoparasites of a wide variety of mainly dicotyledonous plants
(Kreutz, 1995). Members of the Fabaceae and Asteraceae are frequent host plants for
European broomrapes. Few species of Orobanche are parasites of a single host species. O.
hederae and O. elatior are notable exceptions to this general rule, in Britain at least, in
parasitising almost exclusively Hedera helix and Centaurea scabiosa, respectively. Many
though are restricted to a particular genus or closely related genera, the generalist parasites
being very few.

Most work on the biology and ecology of broomrapes has concentrated on the pest
species which parasitise crop plants, mainly in the Mediterranean, North Africa and Middle
East (Weber & Fortstreuter, 1987; Parker & Riches, 1993; Press & Graves, 1995). Those
that have received the greatest attention are O. crenata, O. cernua, O. ramosa and O.
aegyptiaca, and to a lesser extent O. minor. There are various methods of controlling
broomrapes and they include the use of herbicides, germination stimulants, catch or trap
crops, cropping regimes, soil solarization (Abu Irmaileh, 1991), development of resistant
genotypes of crop and diseases of the Orobanche themselves. A review of methods of

Naturalist 123 (1998)

90 The Biology and Ecology of Orobanche: a Bibliographic Review

controlling pest species of Orobanche is given by Dhanapal et al. ( 1996) and they conclude
that integrated management systems are the only effective means of controlling them.

One of the aspects of the biology of Orobanche that has received the greatest attention
concerns the conditions and requirements for seed germination. The results of this work
has shown that seeds of Orobanche require a period of pre-conditioning under moist
conditions for as long as 18 days in some cases (Sauerborn, 1989). The optimum
temperature is between 15 and 20°C and depends on the provenance of the seeds. The
requirement for a pre-conditioning of Orobanche seeds is largely reported from species
found in semi-arid environments (Abu-Shakra, Miah & Saghir, 1970; van Hezewijk et al.,
1993; BarNun & Mayer, 1993).

The seeds require a stimulant after this pre-conditioning in order to germinate, which is
present in exudates or extracts of the roots of its host plant (Brown, 1946; Brown et al.,
1951; Sunderland, 1960a, 1960b; Elghamrawy et al., 1990). Because of the potential for
controlling the pest species of Orobanche by applying these stimulants, a great deal of
work has gone into identifying the chemical stimulant released by the host roots and
examining how effective it is in stimulating germination of their seeds. The stimulant for
germination varies between studies as much as between the different species of Orobanche
tested, but strigol is a ubiquitous stimulant (Spelce & Musselman, 1981). Other chemicals
that appear to be effective in germinating Orobanche seeds are various gibberellic acids,
brassinolide, brassinosteroids, sorgolactone and various strigol analogues (Spelce &
Musselman, 1981; Bergmann et al., 1993; Takeuchi et al., 1995; Thuring et al., 1997a,
1997b, 1997c, 1997d, 1997e). Gibberellic acid appears to stimulate germination if applied
in the pre-conditioning period as well as acting as a replacement for other chemicals that
stimulate germination (Sahai & Shivanna, 1982; Dhanapal & Struik, 1997).

Seeds can remain viable without germinating after the pre-conditioning period (BarNun
& Mayer, 1993; Thuring et al., 1997a and 1997b). Other treatments, including scarification
and treatment with sulphuric acid, have been reported to stimulate germination through
softening the seed coat (Goldwasser et al., 1995; Lopez-Granados and Garcia-Torres,
1996; Mori et al., 1997). Seeds can go into a secondary dormancy phase if they do not
receive a stimulant after the pre-conditioning period.

The most active region of the host root in stimulating germination of Orobanche seeds
appears to be close to the root-tip (Sunderland, 1960b). Increasing concentrations of
nitrogen in the soil have been reported to reduce the infection rate of crops by Orobanche
(Abu Irmaileh, 1981, 1994; Jain, & Foy, 1992), but recent work with O. minor grown on
clover showed an increase in the number of spikes per host plant with increasing nitrogen
levels added to the soil (Dale, pers. comm.). This is probably more related to the root
density in the soil increasing the frequency with which host roots come into contact with
Orobanche seeds, rather than any effects on germination. High concentrations of
ammonium-nitrogen rather than nitrate or urea per se appear to be responsible for the
inhibition of seed germination when applied during the conditioning and germination
phases (van Hezewijk & Verkleij, 1996).

Once germinated, the seeds produce a corkscrew-like radicle that penetrates the host root
by dissolving the walls of its root cells (Shomerilan, 1993; Singh & Singh. 1993),
subsequently forming a haustorium (Sahai & Shivanna, 1981; Joel & Losnergoshen, 1994).
It is through this organ that the parasite derives all its water and nutrients from its host’s
xylem and phloem (Aber & Salle, 1983; Aber, Fer & Salle, 1983; Dorr & Kollmann,
1995). The detailed morphology and processes involved in the infection of host plants by
Orobanche are given by Sahai and Shivanna ( 1981 ) and Press and Graves ( 1995).

The parasite gradually enlarges a tuber outside the host’s root whilst still attached to it.
Once this tuber is sufficiently large, the flowering stem primordium will rapidly swell and
enlarge. The plant accumulates high concentrations of various non-essential sugar alcohols,
particularly mannitol, in order to draw water from its host root system prior to emergence
(Harloff & Wegmann, 1993). Thus the flowering of plants can vary within and between
years at a site depending on the climate and timing of attachment of the Orobanche

The Biology and Ecology o/'Orobanche: a Bibliographic Review 9 1

seedlings to the host’s roots.

Studies have also concentrated on how much damage various species of Orobanche
inflict on a variety of crops (Arjonaberral et ai, 1987; Barker et ai, 1996; Manschadi et al.,
1996; Dhanapal et al., 1997) and various methods of controlling the populations of
Orobanche in fields (Eplee & Norris, 1995; Dhanapal & Struik, 1996; Jurado-Exposito
et al., 1996, 1997; Hershenhorn et al., 1996). The timing of crop sowing has been
shown to affect the infection rate by O. crenata, which decreased in the order
autumn>winter>spring>summer (van Hezewijk et al., 1994; Lopez-Granados & Garcia-
Torres, 1997). Generally, sowing crops earlier in the growing season increases the infection
rate by Orobanche (Mesa-Garcia & Garcia-Torres, 1986). This can be explained by the
pre-conditioning requirement of the seeds for warm and moist conditions, which tend to be
predominant in autumn. A study of the population dynamics of O. crenata showed that the
growth rate of the population was related to rainfall and soil temperatures during December
to February, i.e. the period of crop vegetative growth (Lopez-Granados & Garcia-Torres,

1996) .

The yield of crops such as broad bean can be reduced by as much as 63% when
Orobanche crenata seeds are sown at a density of 600 per kg soil (Manschadi et al., 1996).
The yield of tomato is reduced linearly with increasing seed densities in the soil up to a
maximum of 10 mg dnr3 of soil in the case of O. aegyptiaca (Barker et al., 1996). The
yield of tobacco decreased with an increase in the number of O. cernua spikes per plant.
The weight of the individual spikes of O. cernua decreased as the number of spikes per
host plant increased. This suggests there is intraspecific competition between Orobanche
plants for resources from its host plant (Linke et al., 1991; Lopez-Granados & Garcia-
Torres, 1993a, 1993b). O. crenata parasitising Vicia faba can have a maximum spike
density of 10 to 40 nr2, and not suprisingly the population growth rate is fastest at the
lowest population densities (Lopez-Granados & Garcia-Torres, 1993b; Manschadi et al.\

1997) .

Studies have shown that Orobanche have large and very persistent seed banks in the soil
(Ashworth, 1976; Lopez-Granados & Garcia-Torres, 1993). The seed bank of O. crenata
.can reach four million per m2 with a viability of 53 to 68%. Only 0.003% of seeds become
attached and of these only 9% actually emerge and flower, probably due to lack of nutrients
available from the host plant. The seed output was estimated to be as much as 4 million per
m2 at a spike density of 53 per m2.

Orobanche species are easily killed with glyphosate, but many more herbicides,
including chlorsulfuron, sulfosate, imazethapyr, metham sodium, imidazolines, maleic
hydrazide and mazapyr, are also effective in controlling them (Mesa-Garcia & Garcia-
Torres, 1985; Foy et al., 1988; Jacobsohn et al., 1988; Castejon-Munoz et al., 1990;
( Garcia-Torres & Lopez-Granados, 1991; Kotoulasyka & Eleftherohorinos, 1991; Garcia-
Torres et al., 1994, 1995; Lolas, 1994; Goldwasser et ai, 1995; Gressel, Segel & Ransom,
1996; Jurado-Exposito et al, 1996, 1997). Potential biological control agents such as
various insects and fungi that attack Orobanche have also been investigated (Almenoufi,
1982; Linke et al., 1990, 1992; Raju et al., 1995). There are various models of the
population dynamics of O. crenata and their host plants in a variety of cropping regimes
(Castrotendero & Garcia-Torres, 1995; Garcia-Torres et al., 1996; Schnell et al., 1996;
Lopez-Granados & Garcia-Torres, 1997).

The taxonomy and systematics of Orobanche have to date primarily relied upon
morphology: from habit, pigmentation, etc., through to micro-characters such as seed and
pollen ornamentation (Musselman, 1986; Rumsey & Jury, 1991: Kreutz, 1995, etc.). The
limitations imposed by character loss through reduction associated with parasitism (see
Rumsey. 1998) may be overcome by the application of phytochemical and molecular
techniques; however, little has been published to date on these techniques employed on
Orobanche. Some authors, e.g. Wolfe and de Pamphilis (1997), have concentrated on the
evolutionary aspects of the parasitic condition at the gene level; most, however, have
sought to investigate genetic variation within and among species based on molecular

92

The Biology and Ecology o/ Orobanche: a Bibliographic Review

markers. This work has concentrated on weed species; Verkleij et al. (1986, 1989, 1991,
1994) investigated alloymic variation in O. crenata and O. aegyptiaca in Spain and Syria,
and Paran et al. (1997) used DNA (RAPD) markers to study the five main species in Israel.
Both studies investigated intraspecific variation in relation to host and found no correlation.
The genetic variation within taxa was primarily held within populations as opposed to
between populations. This indicates that high levels of gene flow occur between
populations, which Paran et al. (1997) ascribe to efficient seed dispersal and presumably
not to transfer of pollen between populations. It might be argued, however, that regular
introduction through unwitting human transport is mostly responsible for the patterns of
diversity now witnessed. The advent of quick, relatively cheap DNA methods which
require very little plant material, e.g. the characterisation of RAPD profiles from individual
seeds (Joel, Portnoy & Katzir, 1996; Portnoy et al., 1997), superficially offers great
potential. Care must be taken in the interpretation of such studies using RAPD methods, as
these have been widely criticised for their lack of reproducibility and unknown, and
unknowable genetic basis.

A selected list of recent and pertinent literature on the biology and ecology of species of
Orobanche is given below.

References

Aber, M., Fer, A. and Salle, G. (1983). Transfer of organic substances from the host plant
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Aber, M. and Salle, G. (1983). Ontogenic and ultrastructural study of the primary sucker of
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Abu Irmaileh, M. E. ( 1981 ). Response of hemp broomrape ( Orobanche ramosa) infestation
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Abu Irmaileh, B. E. (1991). Soil solarization controls broomrapes (Orobanche spp.) in host
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Abu Irmaileh, B. E. (1994). Nitrogen reduces branched broomrape ( Orobanche ramosa)
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Abusbaih, H. A., Keithlucas, D. M., Jury, S. L. and Tubaileh, A. S. (1994). Pollen
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Abu-Shakra, S., Miah. A. A. and Saghir, A. R. (1970). Germination of seeds of branched
broomrape ( Orobanche ramosa L.). Horticultural Research 10: 1 19-124.

Almenoufi, O. A. (1982). Studies on Orobanche spp. - fungi associated with Orobanche
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Andary, C., Wylde, R., Laffite, C., Privat, G. and Winlernitz, F. (1982). Structures of
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Arjonaberral, A., Mesa-Garcia, J. and Garcia-Torres, L. (1987). Phenology and growth of
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Barker, E. R., Press, M. C., Scholes, J. D. and Quick, W. P. (1996). Interactions between
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BarNun, N. and Mayer, A. M. (1993). Preconditioning and germination of Orobanche
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BenHod, G., Losner, D., Joel, D. M. and Mayer, A. M. (1991). In vitro culture of
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Bergmann, C., Wegmann, K.. Frischmuth. K.. Samson, E., Kranz, A.. Weigelt, D., Roll, P.
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and structural analogs dependence on constitution and configuration of the germination

93

The Biology and Ecology of Orobanche: a Bibliographic Review

stimulants. Journal of Plant Physiology 142: 338-342.

Brown, R. (1946). Biological stimulation in germination. Nature 157: 64-68.

Brown, R., Greenwood, A. D., Johnson, A. W. and Long, A. G. (1951). The stimulant
involved in the germination of Orobanche minor Sm. I Assay technique and bulk
preparation of the stimulant. Biochemical Journal 48: 559.

Castejon-Munoz, M., Romero-Munoz, F. and Garcia-Torres, L. (1990). Control of
broomrape ( Orobanche cernua) in sunflower ( Helianthus an nuns ) with glyphosate. Crop
Protection 9: 332-336.

Castejon-Munoz, M., Romero-Munoz, F. and Garcia-Torres, L. (1993). Effect of planting
date on broomrape ( Orobanche cernua Loefl) infections in sunflower ( Helianthus
annuus L.). Weed Research 33: 171-176.

Chun, D., Wilhelm, S. and Sagen, J. E. (1979). Components of record germination in vitro
of branched broomrape, Orobanche ramosa L. In: Supplement to the Proceedings of the
Second International Symposium on Parasitic Weeds. L. J. Musselman, A. D. Worsham,
and R. E. Eplee, (eds.) pp. 1-18. North Carolina State University, Raleigh.

Cubero, J. I., Pieterse, A. H., Khalil, S. A. and Suaerborn, J. (1994). Screening techniques
and sources of resistance to parasitic angiosperms. Euphytica 73: 51-58.

Dhanapal, G. N. and Struik, P. C. (1996a). Broomrape ( Orobanche cernua ) control before
attachment to host through chemically or biologically manipulating seed germination.
Netherlands Journal of Agricultural Science 44: 279-29 1 .

Dhanapal, G. N. and Struik, P. C. (1996b). Broomrape control in a cropping system
containing bidi tobacco. Journal of Agronomy and Crop Science 177: 225-236.

Dhanapal, G. N., Struik, P. C. and ter Borg, S. J. (1997). Field observations on interactions
between Orobanche cernua Loefl. and bidi tobacco in Nipani, India. Journal of
Agronomy and Crop Science 179: 83-89.

Dhanapal, G. N., Struik, P. C., Udayakumar, M. and Timmermans, P. C. J. M. (1996).
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Science 176: 335-359.

Dorr, I. and Kollmann, R. (1995). Symplasmic sieve element continuity between
Orobanche and its host. Botanica Acta 108: 47-55.

Edwards, W. G. H. (1972). Orobanche and other plant parasite factors. In: Phytochemical
Ecology. J. B. Harborne, (ed.) pp. 235-248. Academic Press, London.

Elghamrawy, N., Salem, S. M. and Neumann, K. H. (1990). Nature of root exudates of
Vicia fciba plants in relation to induction of Orobanche crenata seed germination.
Angewandte Botanik 64: 215-224.

Eplee, R. E. and Norris, R. (1995). Control of parasitic weeds. In: Parasitic Plants. M. C.
Press and J. D. Graves, (eds.), pp. 256-277 . Chapman & Hall, London.

IFahmy, G. M., Eltantawy, H. and Elghani, M. M. A. (1996). Distribution, host-range and
biomass of 2 species of Cistanche and Orobanche cernua parasitizing the roots of some
Egyptian xerophytes. Journal of Arid Environments 34: 263-276.

Fer, A., Painset, J. C. and Rey, L. (1992). Main features of the mineral nutrition in 3
different parasitic angiosperms growing on crop plants. Bulletin de la Societe Botanique
de France 139: 111-121.

Foy, C. L., Jacobsohn, R. and Jain, R. (1988). Screening of Lycopersicon spp. for
glyphosate and Orobanche aegyptiaca Pers. resistance. Weed Research 28: 383-391.

FFruchier, A., Rascol, J. P., Andary, C. and Privat, G. (1981). A tropone derivative
Orobanche rapum-genistae. Phytochemistry 20: 777-779.

Garcia-Torres, L., Castejon-Munoz, M., Jurado-Exposito, M. and Lopez-Granados, F.
(1996). Modelling the economics of controlling nodding broomrape (Orobanche cernua)
in sunflower (Helianthus annuus). Weed Science 44: 591-595.

Garcia-Torres, L., Castejon-Munoz, M., Lopez-Granados, F. and Jurado-Exposito, M.
(1995). Imazapyr applied postemergence in sunflower (Helianthus annuus) for
broomrape (Orobanche cernua) control. Weed Technology 9: 819-824.

Garcia-Torres, L. and Lopez-Granados, F. (1991). Orobanche crenata (Forsk.) in broad

94 The Biology and Ecology 0/ Orobanche: a Bibliographic Review

bean ( Vicia faba L.) with imidazolinones and other herbicides. Weed Research 31: 227-
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Garcia-Torres, L., Lopez-Granados, F. and Castejon-Munoz. M. (1994). Pre-emergence
herbicides for the control of broomrape (Orobanche cernua Loefl.) in sunflower
( Helianthus annuus L.). Weed Research 34: 395-402.

Goldwasser, Y. (1995). Spinach ( Spinacia oleracea var. attica) as a host of Egyptian
broomrape ( Orobanche aegyptiaca). Phytoparasitica 23: 357-358.

Goldwasser, Y., Kleifeld. Y.. Golan. S., Bargutti, A. and Rubin. B. (1995). Dissipation of
metham-sodium from soil and its effect on the control of Orobanche aegyptiaca. Weed
Research 35: 445-452.

Gonzalez-Torres, R.. Jimenezdiaz. R. M. and Melerovara, J. M. (1982). Distribution and
virulence of Orobanche cernua in sunflower crops in Spain. Journal of Phytopathology
104: 78-89.

Hameed, K. M., Saghir. A. R. and Foy, C. L. (1973). Influence of root exudates in
Orobanche seed germination. Weed Research 13: 114-117.

Harloff, H. J. and Wegmann, K. (1993). Evidence for a mannitol cycle in Orobanche
ratnosa and Orobanche crenata. Journal of Plant Physiology 141: 5 1 3-520.

Hershenhorn, J., Goldwasser, Y., Plakhine, D., Herzlinger, G., Golan, S., Russo, R. and
Kleifeld, Y. (1996). Role of pepper ( Capsicum annuum) as a trap and catch crop for
control of Orobanche aegyptiaca and O. cernua. Weed Science 44: 948-95 1 .

Jacobsohn, R. Benghedalia, D. and Marton, K. (1987). Effect of the animals digestive
system on the infectivity of Orobanche seeds. Weed Research 27: 87-90.

Jacaobsohn. R., Foy, C. L. and Marton, K. (1990). Growing broomrape ( Orobanche spp.)
in a soil-less system. Weed Technology 4: 804-807.

Jacobsohn. R.. Kelman. Y., Shaked. R. and Klein, L. (1988). Broomrape (Orobanche spp.)
control with ethylene dibromide and chloropicrin. Weed Research 28: 151-157.

Jacobsohn, R. and Marcus, R. (1988). Quantitative determination of broomrape
(Orobanche spp.) seeds in vetch seeds. Weed Research 28: 159-162.

Jain. R. and Foy, C. L. (1992). Nutrient effects on parasitism and germination of Egyptian
broomrape (Orobanche aegyptiaca ). Weed Technology 6: 269-275.

Joel, D. M. (1987). Detection and identification of Orobanche seeds using fluorescence
microscopy. Seed Science and Technology 15: I 19-124.

Joel, D. M. and Losnergoshen, D. (1994). The attachment organ of the parasitic
Angiosperms Orobanche cumana and O. aegyptiaca and its development. Canadian
Journal of Botany 72: 564-574.

Joel, D. M.. Portnoy, V. and Katzir, N. (1996). Identification of single tiny seeds of
Orobanche using RAPD analysis. Plant Molecular Biology Reporter 14: 243-248.

Jurado-Exposito, M., Castejon-Munoz, M. and Garcia-Torres, L. (1996). Broomrape
(Orobanche crenata ) control with imazethapyr applied to pea (Pisum sativum) seed.
Weed Technology 10: 774-780.

Jurado-Exposito, M., Garcia-Torres, L. and Castejon-Munoz, M. (1997). Broad bean and
lentil seed treatments with imidazolinones for the control of broomrape (Orobanche
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Katzir, N., Portnoy, V., Tzuri, G., Castejon-Munoz, M. and Joel, D. M. (1996). Use of
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Khalaf, K. A. (1992). Evaluation of the biological activity of flax as a trap crop against
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Kleifeld, Y., Goldwasser, Y., Herzlinger, G., Joel, D. M., Golan, S. and Kahana, D. (1994).
The effects of flax (Linum usitatissimum L.) and other crops as trap and catch crops for
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Kotoulasyka, E. and Eleftherohorinos, I. G. (1991). Orobanche ramosa L. (broomrape)
control in tomato (Lycopersicon esculentum Mill.) with chlorsulfuron, glyphosate and
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Linke, K. H., Scheibel, C., Saxena, M. C. and Sauerborn, J. (1992). Fungi occurring on
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Sauerborn, J. (1989). The influence of temperature on germination and attachment of the
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Sauerborn, J., Linke, K. H., Saxena, M. C. and Koch, W. (1989). Solarization - a physical
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176: 109-115.

97

The Biology and Ecology o/Orobanche: a Bibliographic Review

Spelce, D. L. and Musselman, L. J. (1981). Orobanche minor germination with strigol and
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'Sunderland, N. (1960a). The production of the Striga and Orobanche germination
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'Suzuki, Y„ Ahang, Y. H., Murofushi, N. and Takeuchi, Y. (1994). Endogenous
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13: 63-67.

Takeuchi. Y., Omigawa, Y., Ogasawara, M., Yoneyama, K., Konnai, M. and Worsham,
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Terborg, S. J., Willemsen, A., Khalil, S. A., Saber, H. A., Verkleij, J. A. C. and Pieterse,
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Thalouarn, P„ Theodet, C„ Russo, N. and Delavault, P. (1994). The reduced plastid
genome of a nonphotosynthetic angiosperm Orobanche hederae has retained the rbcl
gene. Plant Physiology and Biochemistry 32: 233-242.

Thuring, J. W. J. F„ Bitter, H. H., de Kok, M. M., Nefkens, G. H. L„ van Riel, A. M. D. A.
and Zwanenburg, B. (1997a). N-phthaloylglycine-derived strigol analogues. Influence of
the D-ring on seed germination activity of the parasitic weeds Striga hermonthica and
Orobanche crenata. Journal of Agricultural and Food Chemistry 45: 2284-2290.

Thuring, J. W. J. F., Heinsman, N. W. J. T., Jacobs, R. W. A. W. M., Nefkens, G. H. L. and
Zwanenburg, B. (1997b). Asymmetric synthesis of all stereoisomers of
dimethylsorgolactone. Dependence of the stimulatory activity of Striga hermonthica and
Orobanche crenata seed germination on the absolute configuration. Journal of
Agricultural and Food Chemistry 45: 507-513.

Thuring, J. W. J. F., Nefkens, G. H. F. and Zwanenburg, B. (1997c). Synthesis and
biological evaluation of the strigol analogue carba-GR24. Journal of Agricultural and
Food Chemistry 45: 1409-1414.

Thuring, J. W. J. F., Nefkens, G. H. F. and Zwanenburg, B. (1997d). Asymmetric synthesis
of all stereoisomers of the strigol analogue GR24. Dependence of absolute configuration
on stimulatory activity of Striga hermonthica and Orobanche crenata seed germination.
Journal of Agricultural and Food Chemistry 45: 2278-2283.

Thuring, J. W. J. F., vanGaal, A. A. M. A., Hornes, S. J., deKok, M. M., Nefkens, G. H. F.
and Zwanenburg, B. (1997e). Synthesis and biological evaluation of strigol analogues
modified in the enol ether part. Journal of the Chemical Society-Perkin Transactions 1:
767-774.

Vail, S. L., Dailey, O. D., Blanchard, E. J., Pepperman, A. B. and Riopel. J. F. (1990).
Terpenoid precusors of strigol as seed germination stimulants of broomrape (Orobanche
ramosa) and witchweed ( Striga asiatica). Journal of Plant Growth Regulation 9: 77-83.

van Hezewijk, M. J., Finke, K. H., Lopez-Granados, F., Almenoufi, O. A., Garcia-Torres,
F., Saxena, M. C., Verkleij, J. A. C. and Pieterse, A. H. (1994). Seasonal changes in
germination response of buried seeds of Orobanche crenata Forsk. Weed Research 34:
369-376.

van Hezewijk, M. J., Van Beem, A. P., Verkleij, J. A. C. and Pieterse, A. H. (1993).
Germination of Orobanche crenata seeds, as influenced by conditioning temperature and
period. Journal of Botany 71: 786-792.

van Hezewijk, M. J. and Verkleij, J. A. C. (1996). The effect of nitrogenous compounds on
in-vitro germination of Orobanche crenata Forsk. Weed Research 36: 395-404.

Verkleij, .1. A. C. and Pieterse, A. H. (1994). Genetic variation of Orobanche (broomrape)

98

Field Note

and Striga (witchweed) in relation to host specificity. In: S. J. Borg, (ed.) Biology and
Management of Orobanche. Proceedings of the Third International Workshop on
Orobanche and related Striga research, pp. 67-79. Royal Tropical Institute, Amsterdam.

Verkleij, J. A. C., Janssen, J. and Pieterse, A. H. (1986). A preliminary study on
isoenzymatic variation in Orobanche crenata and Orobanche aegyptiaca from Syria. In:
S. J. Borg (ed.) Proceedings of a Workshop on the Biology and Control of Orobanche,
pp. 154-159. LH/VPO, Wageningen.

Verkleij, J. A. C., Egbers, W. S. and Pieterse, A. H. (1989). Allozyme variations in
populations of Orobanche crenata from Syria. In: K. Wegmann and L. J. Musselman
(eds.) Proceedings of the International Workshop on Orobanche Research , 19-22 August
1989, pp. 304-317, Obermarchtal.

Verkleij, J. A. C., Koevoets, P., Lopez-Granados, F., Egbers, W. S., Garcia-Torres, L. and
Pieterse, A. H. (1991). Genetic variability in populations of Orobanche crenata from
Spain. In: J. K. Ransom, L. J. Musselman, A. D. Worsham and C. Parker (eds.) Fifth
International symposium on Parasitic Weeds , 24-30 June 1991, pp. 462-469, Nairobi.

Whitney, P. J. (1979) Broomrape seed germination stimulants and inhibitors from host
roots. In: L. J. Musselman, A. D. Worsham and R. E. Eplee (eds.). Proceedings of the
Second International Symposium on Parasitic Weeds, pp. 182-192. North Carolina State
University. Raleigh.

Wink, M.. Witte, L. and Hartmann, T. (1981). Quinolizidine alkaloid composition of plants
and of photomixotrophic cell-suspension cultures of Sarothamnus scoparius and
Orobanche rapum-genistae. Planta Medico 43: 342-352.

Wolfe, A. D. and de Pamphilis, C. W. (1997). Alternate paths of evolution for the
photosynthetic gene rbcl in four nonphotosynthetic species of Orobanche. Plant
Molecular Biology 33: 965-977.

Zeid. M., Madkour, M.. Koraiem, Y., Nawar, A., Soliman, M. and Zailoun, F. (1997).
Molecular studies on Orobanche. Journal of Phytopathology 145: 35 1 -355.

Zwanenburg. B. and Thuring, .1. W. J. F. ( 1997). Synthesis of strigolactones and analogs: a
molecular approach to the witchweed problem. Pure and Applied Chemistry 69: 65 1 -
654.

FIELD NOTE

Two species of Marsh Fly (Diptera: Sciomyzidae) in the Barnsley area

I should like to place on record the occurrence of Coremacera marginata (Fab.) and
Sepedon spltegea (Fab.), two rather local and highly distinctive ‘snail-killing’ flies not
included for this district in Roy Crossley’s excellent review (Notes on the Marsh Flies
(Diptera: Sciomyzidae) of Yorkshire, Naturalist 122: 93-97) recently published.

First recorded locally in 1994, C. marginata is known from three wasteground sites, viz,
Carlton Marsh (SE 3710), Manvers (SE 4501) and Wombwell Ings (SE 4203). It is,
however, perhaps best established at Houghton Common (SE 4308), a sandy tract of birch
scrub and rank grassland.

S. sphegea favours damper places and has been recorded locally since 1989 from Gypsy
Marsh (SE 4102), Smithies (SE 3408), Cortonwood (SE 3901) and Wombwell Ings, this
last site harbours both species, an interesting indication of the often complex habitat
diversity to be found at some ‘mature’ wasteground localities.

Since both species arc readily identified in the field, it is possible that they are currently
undergoing range expansion, particularly C. marginata , which is unlikely to have escaped
notice for so long since regular diptera recording in the district commenced in 1982.

J. D. Coldwell,

16 Railway Cottages, Dodworth, Barnsley S75 3JJ

Ul+WYO \

OBITUARY

JOHN HALLSWORTH FLINT, F.L.A., F.R.E.S. 1919-1997

John Flint at Pocklington Canal, August 1989. Photo: R. Crossley

[ohn Flint, doyen of Yorkshire entomologists, died on 23rd December 1997, and with his
tassing an era of Yorkshire entomology has come to an end.

John Flallsworth Flint was born in Leeds on 6th September 1919. As a boy he lived in
Jpper Armley and was educated at Christ Church and West Leeds High Schools. After
natriculation he joined Leeds City Council’s Public Library Service. He passed his A.L.A.
ixams, with distinction, in 1938, at Leeds College of Commerce and his F.L.A. thesis was
accepted in 1948. He rose through various Branch Librarianships to become Central
^ending Librarian, moving in 1964 to the City’s Education Service to co-ordinate and
establish the library of the embryo Leeds Polytechnic (now Leeds Metropolitan
Jniversity). He retired as Polytechnic Librarian in 1983 and his contribution to its
successful development was acknowledged with the conferment of an Honorary
fellowship of which he was justifiably proud. He spent the war in the army maintaining
adar equipment in the south of England. On one of these radar sites, in 1944, he met Hilda
’Tim’) Steward and they were married in her village church, at Woodham Ferrers in
Sssex, in January 1945. After the war they settled in Chapel Allerton, Leeds.

John’s interest in natural history started early, fostered by his maternal grandfather, and
tis teenage diaries reveal a wide-ranging enthusiasm for birds, plants and insects. This
)road view lasted throughout his life though from the beginning his main interest was
mtomology. His capture of a specimen of the spectacular Velvet-ant, Mutilla europaea, on
he North York Moors in 1937 spurred his mother to find an expert entomologist to help
lim in his hobby. This led to his introduction to the legendary W. Douglas Hincks who
emained a close friend until his untimely death in 1961. Hincks’ influence on the youthful
>eginner was obvious to all who knew John well, for he often spoke of Douglas with great
espect and affection. He introduced him to the Leeds Co-operative Field Naturalists’ Club
nd in 1938 John also joined the Leeds Naturalists’ Club and Scientific Association,
iesides attending meetings of the Entomological Section of the Yorkshire Naturalists’
Jnion which he formally joined in 1940. In these societies he enjoyed the company and
nentorship of other prominent entomologists of the day including John Dibb, J. Digby

100

Obituary

Firth, and T. Basil Kitchen who became another firm friend. In 1944, he was elected a
Fellow of the Royal Entomological Society.

At his request his prize for achieving a distinction in his A.L.A. exams was a copy of
N. H. Joy’s Handbook of British Beetles. This weighty tome travelled with him throughout
the war and he spent every available moment collecting and identifying beetles. He also
studied the haunts and habits of Orthoptera, Heteroptera, Homoptera, aculeate
Hymenoptera and brachyceran and syrphid Diptera. Tim took up Odonata and together
they collected and reared symphytan Hymenoptera, while under John’s guidance their sons,
Peter and Jeremy, also became competent entomologists.

After the war he became actively involved with the Y.N.U. Entomological Section,
being Section Secretary 1953-63, Survey Committee Chairman 1968-73, and Section
Chairman 1973-83; he also served for many years on the Union’s Executive Committee.
He was Recorder, sometimes concurrently, for Coleoptera. Hemiptera and Neuroptera,
assiduously maintaining the Y.N.U. records and regularly producing comprehensive
reports of new and significant discoveries, always preceded by an erudite introduction; his
contributions to the published reports of Union field meetings were always equally
scholarly. He also assisted Tim when she was Hymenoptera Recorder. John was a member
of the Spurn Survey Team in 1951 and 1952, and with Hincks organised the 5-year survey
by the Entomological Section at Malham, 1954-1958, and wrote the introduction to the
report which was published in 1963. John was also a member of the survey team which
worked at Freshfield from 1959-1963. He published many short field notes over the years
in The Naturalist, and also in The Entomologist’s Monthly Magazine between 1946 and
1976, and for many years he was a regular book reviewer for The Naturalist. Involvement
with the Yorkshire Naturalists' (now Wildlife) Trust began in 1964 and John served as a
member of Council from 1965 until 1984. He acted for several years as Potential Reserves
Officer, and it was on the basis of his recommendations in that period that the Trust
pursued the acquisition of a number of properties as reserves. He was also instrumental in
initiating entomological recording on reserves, a task for which he was well suited.

Towards the end of his active fieldwork, John had the pleasure of adding a new insect to
the British List. This was the hopper Cicadula ornata, of which he found several
specimens at Aughton Ings in 1987, and an account of this discovery was published in the
Entomologist’s Gazette (40: 345-346, 1989). What is most remarkable is that identification
depends upon examination of minute internal parts of the insect, demanding delicate
dissection and microscopic examination, and this was at a time when he had difficulty in
controlling the hand trembles that marked the early stages of Parkinson’s disease!

John revelled in the company of fellow enthusiasts and had a special flair for
encouraging beginners, especially those prepared to make a determined effort to get to
grips with their chosen subject. At indoor meetings his exhibition boxes were always
instructive and set a high standard for others to emulate. His full and productive life was
marred towards the end by a prolonged and progressively debilitating illness, but his
influence will last among those fortunate to have known his friendship and wise counsel.
During his lifetime John was honoured by his fellow naturalists in recognition of his
contributions to those organisations he served so loyally: President of the Leeds
Naturalists’ Club and Scientific Association 1951 and 1979; President of the Yorkshire
Naturalists’ Union 1970; Honorary Life Member of the Yorkshire Naturalists’ Union 1994;
Vice-President of the Yorkshire Wildlife Trust 1979-1984 and Honorary Life Vice-
President of the Yorkshire Wildlife Trust 1984.

The respect and affection in which he was widely held was amply demonstrated by the
large attendance at his funeral in Leeds. John enjoyed the unfailing support and
companionship of Tim and she was always the perfect hostess to all who visited their
home and enjoyed their warm hospitality. To Tim, and to Peter, I am indebted for
information about John’s early life, and our condolences are extended to her and the family
in their sad loss.

Ross Crossley

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