1

A global review of weeds that can germinate from horse dung

Michael Ansong* and Catherine Pickering

This article has been published in the journal of Ecological Management and Restoration and

can be cited as:

Ansong, M., & Pickering, C. (2013). A global review of weeds that can germinate from horse

dung. Ecological Management & Restoration, 14(3), 216-223. doi: 10.1111/emr.12057

http://onlinelibrary.wiley.com/doi/10.1111/emr.12057/abstract

*Author for correspondence.

Michael Ansong

Phone +61 7 55528491,

fax: 61 7 5552 8067.

E-mail: michael.ansong@griffithuni.edu.au

Acknowledgements

The authors would like to thank Ann Mount who provided us with original data for use in the

database. One of the authors (Michael Ansong) would like to also acknowledge financial

support from the Griffith University Postgraduate Research Scholarship Scheme

2

Summary

To assess the diversity of weed seeds dispersed via horse dung, we reviewed 15 studies on

seed germination from horse dung – six from Europe, four from North America, three from

Australia and one study each from Africa and Central America. Seed from 249 species from

43 families have been identified germinating from horse dung. Almost two-thirds of the

species were forbs and 33% graminoids; with over half being perennials and 32% annuals.

Nearly every species (totalling 99% of those reviewed) is considered a weed somewhere,

with 47% recorded as invasive, and 19% international environmental weeds. Of the 2,739

non-native plants that are naturalized in Australia, 156 have been shown to germinate from

horse dung. This includes 16 of the 429 listed noxious weeds in Australia, and two weeds of

national significance. Seed from 105 of the 1,596 invasive/noxious plant species in North

America have also been identified germinating from horse dung.

Seed traits including seed size, length, width and mass affect dispersal via horse dung.

Habitat disturbance from trampling facilitates germination of seedlings from dung in both

natural and experimental studies. Some studies found that plants germinating from dung

reach maturity and flower while others found plants did not survive due to unfavourable

growing conditions in the field. The diversity of species with seed that can germinate from

horse dung highlights the potential of horses to disperse a range of seed over long distances.

Whether such dispersal is beneficial or harmful depends on the plant and the context in which

it germinates. In order to maintain the conservation value of protected areas, it is important to

understand and manage the different potential weed dispersal vectors, including horses.

Keywords: Endochory, protected areas, recreational activities, tourism impact, weed

dispersal, zoochory

3

Introduction

Tourism and passive recreation are among the few human activities permitted in many

protected areas (Castley et al. 2009; Newsome et al. 2013). One activity allowed in some

protected areas is horse riding, particularly in developed countries where it has been a

traditional pastime (Landsberg et al. 2001; Newsome et al. 2004; Nimmo & Miller 2007;

Newsome et al. 2008). Unfortunately, riding can have a range of negative environmental

impacts including trampling of soils and vegetation, nutrient addition via dung and urine,

changing hydrology via damage to riverine systems and spreading weed seeds (Whinam et al.

1994; Nimmo & Miller 2007; Pickering & Hill 2007; Newsome et al. 2008; Pickering et al.

2010). Some of these impacts can occur with other recreational activities (Liddle 1997;

Pickering et al. 2010; Newsome et al. 2013) including spreading weed seed on vehicles and

clothing (Pickering & Mount 2010). Horse riding can spread seed on fur, hooves, riders,

equipment and in feed as well as in dung (Whinam et al. 1994; Weaver & Adams 1996;

Campbell & Gibson 2001; Wells & Lauenroth 2007; Quinn et al. 2008; Pickering & Mount

2010). Viable seed in horse dung could germinate and grow along trails, tracks and holding

areas, from where it may spread further into adjacent natural areas (Newsome et al. 2008;

Pickering & Mount 2010; Quinn et al. 2010).

Weeds are a major threat to biodiversity globally (Williams & West 2000; Weber 2003;

Groves et al. 2005). They compete with native plants for resources such as light and

nutrients, often resulting in reductions in the distribution of native plants (Williams & West

2000; Groves et al. 2005). While there are some cases where particular weeds can be useful

‘bridging’ or ‘substitute habitat in degraded systems, in general, weeds alter habitat quality of

sites for native animals, with some directly affecting animals by poisoning (Williams & West

2000). They also have a range of economic impacts, including increased management costs

and reduced ecosystem services (Williams & West 2000; Groves et al. 2005).

The capacity for propagules (seeds) to be dispersed is a critical step in biological invasions

(Pyšek & Richardson 2010). Due to the high risks and costs associated with the spread of

weeds, information on activities that could disperse weeds in protected areas is important.

More generally there is increasing interest in unintentional long distance seed dispersal by

humans and domesticated animals including horses (Higashino et al. 1983; Lonsdale & Lane

1994; Cosyns et al. 2006; Pickering & Mount 2010; Pickering et al. 2011; Stroh et al. 2012;

Taylor et al. 2012; Ansong & Pickering 2013; Auffret & Cousins 2013; von der Lippe et al.

4

2013). This research includes studies on weed seed dispersal into and within protected areas

(Higashino et al. 1983; Lonsdale & Lane 1994; Cosyns et al. 2006; Pickering & Mount 2010;

Pickering et al. 2011; Stroh et al. 2012; Ansong & Pickering 2013). A review of seed

dispersal by vehicles, clothing, donkeys and horses found that they can disperse a wide

variety of seed over long distances (Pickering & Mount 2010). For instance, seed from 216

species can germinate from horse and donkey dung, including seed from 45 international

environmental weeds (Pickering & Mount 2010).

To inform the management of horses in natural areas, we undertook a comprehensive review

of studies analysing the potential for weed dispersal via horse dung. We examined these in

relation to the following issues: (1) Which species have seed that germinates from horse

dung? (2) How many of these are weeds in Australian and North America? (3) How much

seed can germinate from horse dung? (4) What plant and seed traits favour dispersal via horse

dung? (5) How long can seeds remain viable in the gut of a horse? and (6) Can the seed

germinate, grow and reproduce in protected areas? To answer these questions, we reviewed

the published literature on seed dispersal via horse dung, including updating and expanding

an existing database, to identify which species have seeds that have been recorded

germinating from horse dung (Pickering & Mount 2010).

Methods

Information on the diversity of species with seed that germinate from horse dung and their

weed status was extracted from an existing database (Pickering & Mount 2010). The database

included the results of 13 original research studies published in refereed journals identified

using searches of scientific publication electronic databases. First we removed data from two

studies of seed from fur, one study that recorded seed from donkey dung, and one study that

did not find weed seed germinating from horse dung. We then added data from six new

studies located using searches from April 2012 to May 2013 of the same electronic databases

as Pickering & Mount (2010). This involved searching Science Direct, Web of Science,

Scopus, and Google Scholar using a combination of keywords including tourists, visitors,

horses, dung, recreation, weeds, seeds, diaspores, spread, endozooch* and disper*. Of the 10

additional studies initially identified in these searches, we excluded four of them (Vander

Noot et al. 1967; Cosyns et al. 2005; Loydi & Zalba 2009; Törn et al. 2010) from inclusion

in the database, but not from the general review if the dung could have been contaminated

with seed from the site where it was deposited, if they repeated data in one of the existing

5

studies, or if the study did not find germination of seed from horse dung. The updated

database, therefore, only contained studies that listed the scientific names of seed germinated

from horse dung and minimised the potential for contamination of the dung once deposited

(Table 1).

Insert Table 1 near here

Data from each of the remaining 15 studies that fitted the criteria listed above were included

in the database. Factors included the location in which the research was conducted (continent

and country); the sampling design (including whether it was a manipulative or natural

experiment, or incidental observation); whether the dung was from a protected area; whether

the seeds were germinated in glasshouses, gardens and/or the field; the total number of

species recorded as germinating; and, the total number of species listed in the publication.

The 15 studies from 1934 and 2013 included one study from Africa, one from Central

America, three from Australia, four from North America and six from Europe (Table 1). The

methods used included: (i) collecting fresh (0-4 days old) dung then germinating seed from

the dung in glasshouses; and/or (ii) recording seedlings that germinated from dung in situ.

Some also examined how long seedlings survived in the grazing areas (Whinam et al. 1994;

Weaver & Adams 1996; Campbell & Gibson 2001; Cosyns et al. 2006) and/or whether

trampling increased germination rates (Whinam et al. 1994; Cosyns et al. 2006; Törn 2007).

In four studies (Harmon & Keim 1934; Janzen 1981; St John-Sweeting & Morris 1991; Van

Dyk & Neser 2000), horses were deliberately fed seed from particular species, to determine

retention time and viability of seeds when excreted. In others, dung was collected from areas

where horses are ridden and/or are able to graze within and outside protected areas rather

than areas where horses were stabled or hand fed. Eight studies collected horse dung from

protected areas (Whinam et al. 1994; Weaver & Adams 1996; Campbell & Gibson 2001;

Cosyns & Hoffmann 2005; Wells and Lauenroth 2007; Cosyns et al. 2006; Törn 2007; Stroh

et al. 2012). In all 15 studies, contamination of the dung with new seed was minimised by

removing any parts of dung in contact with the ground, and often by removing the top layer

of the dung prior to germination in glasshouses. Most, but not all of the studies recorded if

they were weeds or native to the region.

We then updated data for all the species identified by their scientific names that were

recorded as germinating from dung in one or more of the 15 studies. We only included

presence/absence data for each species due to variation in the methods used, data reported,

6

duration and location of the studies. The following information was recorded for each species

in the database: continent of origin, growth form and life span. This information was sourced

from PlantNET (Royal Botanic Gardens and Domain Trust 2012), the United States

Department of Agriculture (GRIN Taxonomy for Plants 2012) and Weber (2003). Plant

nomenclature conforms to PlantNET (Royal Botanic Gardens and Domain Trust 2012) and

the United States Department of Agriculture (GRIN Taxonomy for Plants 2012).

We recorded the species’ weed status including whether it is a weed in one or more countries

(Global Compendium of Weeds, Randall 2012) and if it is an internationally important

environmental weed (Weber 2003). We then assessed the species’ weed status in North

America and Australia where horse riding in protected areas remains contentious (Campbell

& Gibson 2001; Nimmo & Miller 2007). We determined whether the species were: (1)

invasive/noxious in North America, (2) introduced to Australia, (3) naturalized in Australia,

(4) declared a noxious weed by a state or territory government in Australia and (5) one of the

32 weeds of national significance in Australia. For North American, we used the list of 1596

species of invasive/noxious weeds in North America produced by the Centre for Invasive

Species and Ecosystem Health from the University of Georgia, and the United States

Department of Agriculture (USDA) Animal and Plant Health Inspection Service

(Invasive.org 2010). For Australia, weed status information was obtained from The List of the

Introduced Flora of Australia and Their Weed Status (Randall 2007) which lists 2,739

naturalised weeds in Australia. We also used the list of 429 species that are declared noxious

weeds in one or more state or territory governments in Australia (Australian Weeds

Committee 2012a) – as well as the list of 32 weeds of national significance (i.e. those which

are considered to be the most problematic invasive weeds by the Australian Government

(Australian Weeds Committee 2012b)).

The database was then used to calculate the number of species that have viable seeds able to

be dispersed via horse dung, their growth forms, life histories and weed status.

Results

(1) Which species have seed that germinate from horse dung?

A total of 249 species from 43 families have seed that germinate from horse dung based on

the database of 15 studies (Table 2). Many were Poaceae (grasses, 22%), Asteraceae (daises,

12%) and Fabaceae (peas, 8%). Almost three quarters of the species were only recorded in a

7

single study, while six species were common across studies. These were White Clover

(Trifolium repens, 9 studies), Winter Grass (Poa annua, 8), Toad Rush (Juncus bufonius, 7),

Sorrel (Acetosella vulgaris, 6), Kentucky Bluegrass (Poa pratensis, 6) and Lamb’s Tongue

(Plantago lanceolata, 6) (Appendix 1). They are all common species in many regions,

including in pastures where horses may graze, which may account for their frequency among

the different studies.

Inert Table 2 near here

(2) How many of these species are weeds in Australian and North America?

Of the studies in the database seven listed the names of weeds and species native to the

region germinating from dung. This included studies from Australia (St John-Sweeting &

Morris 1991) North America (Campbell & Gibson 2001; Wells and Lauenroth 2007; Quinn

et al. 2008) and Europe (Törn 2007; Auffret & Cousins 2013). Four studies recorded only the

names of weeds/exotic species including, studies from North America (Harmon & Keim

1934), Australia (Whinam et al. 1994; Weaver & Adams 1996) and Africa (Van Dyk &

Neser 2000). Three of the European studies only reported natives germinating (Cosyns &

Hoffmann 2005; Mouissie et al. 2005; Stroh et al. 2012) while two studies one from Central

America (Janzen 1981) and one from Europe (Cosyns et al. 2006) did not specify if species

recorded were weeds or native. Gower (2008) found that no weeds germinated from dung

that had been taken from a paddock and then placed along horse trails in a protected area in

the USA, although some native species did germinate. As this study did not list the names of

these native species, we could not include them in the database of species germinating from

dung.

Nearly every species in the database is cited as a weed (99%) in some part of the world

(Randall 2012). Many are globally invasive species (Tables 2 and Appendix 1), with 47% of

the species invasive somewhere in the world (Randall 2012), and 47 species international

environmental weeds (Weber 2003).

Many of these are weeds in North America, with 105 of the 1596 invasive/noxious plant

species in North America (Invasive.org 2010) germinating from horse dung. Of these, 47

species were recorded in one or more of the North American studies (Table 1). The three

North American studies that assessed horse dung from protected areas (Campbell and Gibson

8

2001; Wells & Lauenroth 2007; Quinn et al. 2008) all found invasive species germinating

from the dung.

Quinn et al. (2008) investigated seeds germinating from horse dung from different national

parks, recreation areas and trail heads in central and northern California. They recorded 32

species germinating in an enclosed sterilized nursery, of which 55% are invasive/noxious

weeds in North America (Table 1). Wells and Lauenroth (2007) collected 12 samples of fresh

dung from a horse riding trail in White River Forest, in the Rocky Mountains of Colorado. A

total of 564 seedlings from 20 species germinated in a greenhouse from the dung, of which 7

were invasive/noxious in North America. Campbell and Gibson (2001) assessed the

relationship between the spread of exotic species and recreational horse riding along horse

trails in three reserves of southern Illinois. A total of 66 species, of which 36% are invasive in

North America, germinated in a glasshouse from fresh dung (0–2 days old), collected from

the reserves and one ranch with access to one of the reserves. When vegetation along the

trails was also assessed, only one species exotic to North America, Japanese Clover

(Kummerowia striata), was found growing on the trails.

Of the 2,739 naturalized plants in Australia, 156 (6%) germinate from horse dung. Of the 429

noxious weeds in Australia, 16 have viable seed in horse dung, including two weeds of

national significance, the willows Salix nigra and Salix cinerea. All six of the most common

species found in the studies are naturalized in Australia (Appendix 1) and hence could be

dispersed in horse dung in Australia if their seed is eaten by horses. Across the three

Australian studies, 32 species are naturalized in Australia, and 17 are environmental weeds.

Two of the Australian studies directly assessed weeds in horse dung from protected areas

(Whinam et al. 1994; Weaver & Adams 1996). Whinam et al. (1994) found more weeds in

quadrats where grazing was excluded and soil was disturbed when they assessed impact of

horse trampling and dung in the Tasmanian Wilderness World Heritage Area. Seeds from 10

weed species, all naturalized in Australia, germinated in the field; eight of which are

international environmental weeds (Weber 2003). Weaver and Adams (1996) germinated

seed in glasshouses from dung collected in recreational horse riding tracks and holding pens

in three Victorian National Parks. Seeds from 24 weed species germinated, all of which are

naturalized in Australia (Table 1). The most abundant species, Winter Grass (Poa annua) and

Hare’s-foot Clover (Trifolium arvense), germinated from dung from all the sampled

9

tracks/holding pens. Seeds from 40% of the weeds growing along track verges germinated

from horse dung, indicating that the sites were suitable for these species to establish.

3) How much seed can germinate from horse dung?

Several studies have found large amounts of viable seed in horse dung, with estimates of 700

viable seeds produced per horse per day (St John-Sweeting & Morris 1991) and half a million

seeds per horse per year (Mouissie et al. 2005). Other estimates include an average of 901

seeds per kg of dry dung for free ranging ponies in a field in the Netherlands (Mouissie et al.

2005), 212 seeds per kg of dry dung for free-roaming Konik horses grazing vegetation at

Wicken Fen National Nature Reserve, UK (Stroh et al. 2012) and 382 seedlings per litre of

dung for horses in four dune nature reserves along the Northern French and Belgian coast

(Cosyns & Hoffmann 2005).

(4) What plant and seed traits favour dispersal via horse dung?

Based on the database of species, we found clear patterns in terms of growth form and life

history (Appendix 1). Almost two-thirds of the species germinating from dung were forbs,

33% were graminoids, while only four shrubs and six trees germinated. Over half the species

were perennials and 32% were annuals (Table 2). Individual studies have found that seed

traits such as size, mass/weight and seed coat hardness affect the number of seed dispersed

via horse dung. St John-Sweeting & Morris (1991) and Auffret & Cousins (2013)

demonstrated that smaller seeds (e.g. Balansa Clover (Trifolium michelianum) and

Marshmallow (Althea officinalis)) were more likely to germinate from horse dung compared

to the larger seeds of Horehound (Marrubium vulgare) and Subterranean Clover (Trifolium

subterraneum). Cosyns & Hoffmann (2005) found that the length, width and mass of seed

were negatively correlated with relative seed density in dung. Mouissie et al. (2005) found

lighter seeds germinated more frequently than heavier seeds from dung which is similar to

result of Stroh et al. (2012). The hardness of the seed coat can also influence the ability of the

seed to remain viable after passing through the guts of horses, with seeds having hard coats

more likely to be viable when excreted than those with softer seed coats (St John-Sweeting &

Morris 1991). On the other hand, specific shapes of seed do not appear to affect the

probability of seed being dispersed in dung (Cosyns & Hoffmann 2005; Mouissie et al. 2005;

Stroh et al. 2012). Seeds dispersed in horse dung were found by Auffret & Cousins (2013) to

have similar dispersal traits to those transported by motor vehicles. Dung can contain seeds of

plants associated with fertile rather than infertile soils (Moussie et al. 2005), and seed that

10

persist in soil (Auffret & Cousins 2013). The survival of seedlings germinating from horse

dung was also affected by plant traits. Cosyns et al. (2006) found that survival rates varied

over time depending on whether the plants were monocots or dicots, with more monocot

seedlings recorded three months post germination; but better survival rates after that were

found for dicot seedlings, resulting in a higher cover of dicots one year after they germinated.

(4) How long cans seeds remain viable in the gut of horses?

A few studies specifically examined how long after a horse has eaten seed, it may be

excreted. They found that the critical time for the dispersal of seeds was 18 hours to 5 days

after ingestion of the seeds (St John-Sweeting & Morris 1991; Van Dyk & Neser 2000)

although viable seed was still present in dung produced 10-70 days after the seeds were

ingested (Janzen 1981; St John-Sweeting & Morris 1991).

(5) Can the seed germinate, grow and reproduce in protected areas?

Eight of the studies of dung collected from protected areas (Table 1) found germinating seed

included species native to the region (Campbell & Gibson 2001; Cosyns & Hoffmann 2005;

Wells and Lauenroth 2007; Törn 2007 Stroh et al. 2012) as well as weeds (Whinam et al.

1994; Weaver & Adams 1996; Campbell & Gibson 2001; Wells and Lauenroth 2007; Törn

2007). Some that tested germination of seeds from horse dung in the same protected area

where the dung were collected found that seed could germinate in the field from a diversity of

weeds (Whinam et al. 1994; Weaver & Adams 1996; Campbell & Gibson 2001) as well as

native species (Campbell & Gibson 2001; Cosyns et al. 2006). Some studies found that plants

germinating from dung went on to reach maturity and flower (Whinam et al. 1994; Mouissie

et al. 2005), while others found that the plants did not survive due to unfavourable growing

conditions (Campbell & Gibson 2001; Gower 2008). Trampling and soil disturbance both

facilitated germination of seedlings from horse dung in natural and experimental studies

(Whinam et al. 1994; Cosyns et al. 2006; Törn 2007).

Discussion

Seeds from a wide diversity of species can germinate from horse dung including those that

may be native to the region, but also weeds. Further, many of the species were unique to a

given study, indicating that additional research is likely to increase the total number of

species found to germinate from horse dung. Based on the results so far, seed dispersal in

horse dung is a selective mechanism that favours some species over others. Horse dung is

11

more likely to contain species with smaller seeds, predominantly forbs and graminoids, but

rarely the seed of shrubs or trees. These patterns are likely to reflect the combined effects of

the probability of the horses eating the seed deliberately or as a contaminant of feed, the

probability of the seed surviving the transit through the horse, and the germination

requirements of the seed.

Whether seed dispersal by horses is beneficial or harmful depends on the plant species and

the context in which it germinates. Four of the five studies from Europe used in the database

were undertaken specifically to assess the perceived benefits (in Europe) of native seed

dispersal by horses as a way of maintaining high plant diversity among increasingly isolated

protected areas, particularly for ecosystems adapted to grazing by large mammals (Mouissie

et al. 2005; Cosyns et al. 2006; Stroh et al. 2012; Auffret & Cousins 2013). By dispersing

seed over long distances horses were seen as helping to conserve biodiversity in remnant

vegetation and were often deliberately transported among protected areas for this reason

(Mouissie et al. 2005; Cosyns et al. 2006; Stroh et al. 2012; Auffret & Cousins 2013). In

contrast, the large number of Australian and North America weed species germinating from

horse dung is of concern, particularly for protected area managers in these regions. Several of

the studies in both these regions were undertaken specifically to address the risk of weed

spread in dung (Whinam et al. 1994; Weaver and Adams 1996; Campbell & Gibson 2001;

Wells & Lauenroth 2007; Quinn et al. 2008). Nearly all the species found to germinate from

dung are weeds somewhere, and many are major invasive species. Although all 15 studies

that listed the name of species germinating from dung included species classified as weed,

nine of the studies also recorded species native to the region germinating from dung including

some of these conducted in protected areas. There was also another study not included in the

database that only found native species germinating from horse dung (Gower 2008).

Where weeds do germinate from dung, it is possible that the plants may not achieve maturity

and set seed, particularly as dung tends to contain seeds of plants associated with fertile soils

(Mouissie et al. 2005) and Australia soils are often infertile. Even if they do survive, they

may not establish self-perpetuating populations. Varying outcomes have been found in the

studies that assessed the fate of seedlings in the ‘wild’ (Whinam et al. 1994; Weaver &

Adams 1996; Campbell & Gibson 2001; Cosyns et al. 2006). Some found high diversity and

number of seeds germinating from horse dung with some continuing to grow and reach

maturity (Whinam et al. 1994; Mouissie et al. 2005; Cosyns et al. 2006) particularly where

sites are disturbed by trampling (Whinam et al. 1994; Cosyns et al. 2006; Törn 2007). Other

12

studies, however, found that the seed germinated but plants did not reach maturity (Campbell

& Gibson 2001; Gower 2008). Establishment of plants is difficult for both natives and non-

natives, but the presence of weeds along many horse trails demonstrates that some weeds are

able to grow and spread in these locations (Whinam et al. 1994; Törn 2007).

Some key questions remain: how much risk do viable weed seeds in horse dung pose,

particularly in protected areas? Does the level of risk differ among recreational activities?

And what methods should be implemented to reduce the risk? Although, the current study

cannot answer these questions, it has demonstrated that many weeds including invasive

species in North America and Australia can be dispersed by horse dung. As propagule

pressure is considered to be an important factor affecting plant invasions (Pyšek &

Richardson 2010), the precautionary principle suggests that the risk of introducing non-native

seed via horse dung should be minimized.

Implications for management

Protected areas are the main mechanism for the conservation of biodiversity globally

(Newsome et al. 2013), and weeds are a major threat to biodiversity (Csurches & Edward

1998; Williams & West 2000). Guidelines for horse riding in protected areas need to be

framed within the context of the risk that horse dung can contain viable seed of invasive

weeds. In areas where horse riding is permitted, minimum impact codes and codes of conduct

need to be developed by protected area agencies and implemented and adhered to by horse

riders to reduce this risk (Newsome et al. 2004; Newsome et al. 2008). This could include

feeding horses with food that is free of seed (Newsome et al. 2008) at least 42 hours prior to

entry, but preferably longer. Cleaning of horses’ hooves and ensuring their coats and tackle

(as well as vehicles and riders’ clothing) are clean prior to entry would also aid in reducing

weed seed spread. Similar hygiene methods can also be used to minimise the risk of hikers

and vehicles also dispersing weed seed in protected areas (Pickering & Mount 2010;

Pickering et al. 2011; Taylor et al. 2012). In other protected areas where horse riding is not

permitted, the risks of weed dispersal and other impacts of horse riding are judged as too

high.

Conclusion

In this review, we have highlighted the potential range of species that can germinate from

horse dung that are weeds somewhere in the world, many of which are naturalized in

13

Australia and invasive in North America. In order to maintain the conservation value of

protected areas, it is important to understand and manage the different potential dispersal

vectors of weeds, including horses. What is also clear is that more research is required on the

potential of weed seeds to germinate and establish in protected areas, and the success of

different methods to reduce the risk of weeds being spread by horses and other tourist

activities. These studies require time and resources, but help in assessing the appropriateness

of different recreational activities in protected areas including horse riding.

References

Ansong M. and Pickering C. (2013) Long-distance dispersal of Black Spear Grass

(Heteropogon contortus) seed on socks and trouser legs by walkers in Kakadu

National Park. Ecological Management and Restoration 14, 71-74.

Auffret A. G. and Cousins S. A. O. (2013) Grassland connectivity by motor vehicles and

grazing livestock. Ecography 36, 001-008.

Australian Weeds Committee (2012a) Noxious Weed List for Australian States and

Territories. Accessed from http://www.weeds.org.au/noxious.htm, August 2012.

Australian Weeds Committee (2012b) Weeds of National Significance. Accessed from

http://www.weeds.org.au/WoNS, August, 2012.

Campbell J.E. and Gibson D.J. (2001) The effect of seeds of exotic species transported via

horse dung on vegetation along trail corridors. Plant Ecology 157, 23-35.

Castley C., Hill W. and Pickering C.M. (2009) Developing ecological indicators of visitor use

of protected areas: a new integrated framework from Australia. Australasian Journal

of Environmental Management 16, 14-25.

Cosyns E., Bossuyt B., Hoffmann M., Vervaet H. and Lens L. (2006) Seedling establishment

after endozoochory in disturbed and undisturbed grasslands. Basic and Applied

Ecology 7, 360-369.

Cosyns E., Claerbout S., Lamoot I. and Hoffmann M. (2005) Endozoochorous seed dispersal

by cattle and horse in a spatially heterogeneous landscape. Plant Ecology 178, 149-

162.

Cosyns E. and Hoffmann M. (2005) Horse dung germinable seed content in relation to plant

species abundance, diet composition and seed characteristics. Basic and Applied

Ecology 6, 11-24.

Groves R. H., Lonsdale M. and Boden R. (2005) Jumping the garden fence: invasive garden

plants in australia and their environmental and agricultural impacts. WWF-Australia.

Acessed from http://www.weeds.org.au/docs/jumping_the_garden_fence.pdf,

November, 2012.

Gower S. T. (2008) Are horses responsible for introducing non-native plants along forest

trails in the eastern United States? Forest Ecology and Management 256, 997-1003.

GRIN Taxonomy for Plants (2012) USDA, ARS, National Genetic Resources Program.

Germplasm Resources Information Network-Online Database. National Germplasm

Resources Laboratory, Beltsville, Maryland. Acessed from http://www.ars-

grin.gov/cgi-bin/npgs/html/taxgenform.pl, various dates, 2012.

14

Harmon G. W. and Keim F. (1934) The percentage and viability of weed seeds recovered in

the feces of farm animals and their longevity when buried in manure. Agronomy

Journal 26, 762-767.

Higashino P. K., Guyer W. and Stone C. P. (1983) The Kilauea wilderness marathon and

crater rim runs: sole searching experiences. Hawaiian Botanical Society 22, 25–28.

Invasive.org (2010) Invasive and Exotic Plants. Accessed from http://www.invasive.org,

April, 2013.

Janzen D. H. (1981) Enterolobium cyclocarpum seed passage rate and survival in horses,

Costa Rican pleistocene seed dispersal agents. Ecology 62, 593-601.

Landsberg J., Logan B. and Shorthouse D. (2001) Horse riding in urban conservation areas:

reviewing scientific evidence to guide management. Ecological Management &

Restoration 2, 36-46.

Liddle M. (1997) Recreation Ecology. Chapman and Hall, London.

Lonsdale W. M. and Lane A. M. (1994) Tourist vehicles as vectors of weed seeds in Kakadu

National Park, Northern Australia. Biological Conservation 69, 277-283.

Loydi A. and Zalba S. (2009) Feral horses dung piles as potential invasion windows for alien

plant species in natural grasslands. Plant Ecology 201, 471-480.

Mouissie A. M., Vos P., Verhagen H. M. C. and Bakker J. P. (2005) Endozoochory by free-

ranging, large herbivores: ecological correlates and perspectives for restoration. Basic

and Applied Ecology 6, 547-558.

Newsome D., Cole D.N. and Marion J.L. (2004) Environmental impacts associated with

recreational horse-riding. In: Environmental Impacts of Ecotourism (ed.. R. Buckley)

pp. 61-82. CABI International, New York.

Newsome D., Moore S. and Dowling R. (2013) Natural Area Tourism: Ecology, Impacts and

Management. Channel View Publications, Sydney.

Newsome D., Smith A. and Moore S. A. (2008) Horse riding in protected areas: a critical

review and implications for research and management. Current Issues in Tourism 11,

144-166.

Nimmo D. G. and Miller K. K. (2007) Ecological and human dimensions of management of

feral horses in Australia: a review. Wildlife research 34, 408-417.

Pickering C. M. and Hill W. (2007) Impacts of recreation and tourism on plant biodiversity

and vegetation in protected areas in Australia. Journal of Environmental

Management 85, 791-800.

Pickering C. M., Hill W., Newsome D. and Leung Y.F. (2010) Comparing hiking, mountain

biking and horse riding impacts on vegetation and soils in Australia and the United

States of America. Journal of Environmental Management 91, 551-562.

Pickering C.M. and Mount A. (2010) Do tourists disperse weed seed? A global review of

unintentional human-mediated terrestrial seed dispersal on clothing, vehicles and

horses. Journal of Sustainable Tourism 18, 239-256.

Pickering C. M., Mount A., Wichmann M. C. and Bullock J. M. (2011) Estimating human-

mediated dispersal of seeds within an Australian protected area. Biological Invasions

13, 1869-1880.

Pyšek P. and Richardson D. M. (2010) Invasive species, environmental change and

management, and health. Annual Review of Environment and Resources 35, 25-55.

Quinn L. D., Kolipinski M., Coelho V. R., Davis B., Vianney J.M., Batjargal O., Alas M. and

Ghosh S. (2008) Germination of invasive plant seeds after digestion by horses in

California. Natural Areas Journal 28, 356-362.

Quinn L. D., Quinn A., Kolipinski M., Davis B., Berto C., Orcholski M. and Ghosh S. (2010)

Role of horses as potential vectors of non-native plant invasion: an overview. Natural

Areas Journal 30, 408-416.

15

Randall R.P. (2007) The Introduced Flora of Australia and its Weed Status. CRC for

Australian Weed Management. Department of Agriculture and Food, Western

Australia, Perth.

Randall R.P. (2012) A Global Compendium of Weeds. 2nd Edition. Department of

Agriculture and Food, Western Australia, Perth.

Royal Botanic Gardens and Domain Trust (2012) PlantNET - The Plant Information Network

System of The Royal Botanic Gardens and Domain Trust, Sydney(version 2).

Accessed from http://plantnet.rbgsyd.nsw.gov.au, various dates, 2012.

St John-Sweeting R. and Morris K. (1991) Seed transmission through the digestive tract of

the horse. In: Plant Invasions: The Incidence of Environmental Weeds in Australia (ed

S. E. Humphries) pp. 170-172. Australian National Parks and Wildlife Service,

Canberra.

Stroh P.A., Mountford J.O. and Hughes F.M.R. (2012) The potential for endozoochorous

dispersal of temperate fen plant species by free-roaming horses. Applied Vegetation

Science 15, 359-368.

Taylor K., Brummer T., Taper M. L., Wing A. and Rew L. J. (2012) Human-mediated long-

distance dispersal: an empirical evaluation of seed dispersal by vehicles. Diversity and

Distributions 18, 942-951.

Törn A. (2007) Sustainability of Nature Based Tourism (PhD thesis). University of Oulu,

Finland.

Törn A., Siikamäki P. and Tolvanen A. (2010) Can horse riding induce the introduction and

establishment of alien plant species through endozoochory and gap creation? Plant

Ecology 208, 235-244.

Vander Noot G. W., Symons L. D., Lydman R. K. and Fonnesbeck P. V. (1967) Rate of

passage of various feedstuffs through the digestive tract of horses. Journal of Animal

Science 26, 1309-1311.

Van Dyk K. and Neser S. (2000) The spread of weeds into sensitive areas by seeds in horse

faeces. Journal of South African Veterinary Association 71, 173-174.

von der Lippe M., Bullock J. M., Kowarik I., Knopp T. and Wichmann M. (2013) Human-

mediated dispersal of seeds by the airflow of vehicles. PLoS One 8, e52733.

Weaver V. and Adams R. (1996) Horses as vectors in the dispersal of weeds into native

vegetation. In: Eleventh Australian Weeds Conference (ed R. Shepherd) pp. 383-397.

Weed Science Society of Victoria, Melbourne.

Weber E. (2003) Invasive Plant Species of the World: A Reference Guide to Environmental

Weeds. CABI Publishing, New York.

Wells F.H. and Lauenroth W.K. (2007) The potential for horses to disperse alien plants along

recreational trails. Rangeland Ecology and Management 60, 574-577.

Whinam J., Cannell E.J., Kirkpatrick J.B. and Comfort M. (1994) Studies on the potential

impact of recreational horse riding on some alpine environments of the Central

Plateau, Tasmania. Journal of Environmental Management 40, 103-117.

Williams J. and West C.J. ( 2000) Environmental weeds in Australia and New Zealand:

issues and approaches to management. Austral Ecology 25, 425-444.

16

Table 1. Details of 15 research studies that examined seed germinating from horse dung and the weed status of the species identified, globally

and in Australia.

Studies

Detail of methods used in study Weed status

globally Weed status in Australia Invasive/noxious

in North

America In PA?

Study

Type

Method

of Id # taxa

#

species Weed

Enviro.

weed

Naturalized Invasive Noxious

Africa

Van Dyk and Neser . (2000) N ME DI, GG 3 3 3 - 3 - - -

Australia

St John-Sweeting and Morris (1991) N ME DI, GG 6 6 6 3 5 - 2 5

Whinam et al. (1994) Y ME GF 10 10 10 8 10 - - 9

Weaver and Adams (1996) Y NE GG 29 24 24 11 24 - 1 15

Central America

Janzen (1981) N ME DI,GG 1 1 1 - - - - -

North American

Harmon and Keim (1934) N ME DI,GG 7 6 6 2 5 - 2 3

Campbell and Gibson (2001) Y ME GG, GF 77 66 66 7 33 1 5 24

Wells and Lauenroth (2007) Y NE GG 20 17 17 4 10 - - 7

Quinn et al. (2008) Mixed NE GG, GF 32 31 28 8 24 - 2 17

European

Cosyns and Hoffmann (2005) Y NE GG 106 71 69 19 56 3 4 36

Mouissie et al. (2005) N NE GG 35 35 35 11 24 1 - 16

Cosyns et al. (2006) Y NE GG 49 9 9 2 9 1 - 5

Törn (2007) Y ME GF 12 8 8 3 5 1 - 4

Stroh et al. (2012) Y NE GG 41 41 41 11 33 2 2 16

Auffret & Cousins (2013) N NE GG 49 48 48 12 33 - 1 29

In PA (protected area): N = study not conducted in a protected area, Y = study conducted in a protected area, Mixed: dung from protected areas and other sites; Study Type:

NE = Natural experiment, ME = Manipulative experiment; Method of identification: GG = seed germinated in glasshouse, GF = seed germinated in the field, DI = direct

identification of seed; # taxa = number of species, genera and morphotaxa listed in source. # Species = total number of species identified. A weed if listed in Global

Compendium of Weeds (Randall 2012), Environmental weed if listed in ‘Invasive Plant Species of the World’ (Weber 2003). Weed status in Australia: ‘Naturalized’ and

‘Invasive’ if stated in ‘The Introduced Flora of Australia and its Weed Status (Randall 2007); Noxious if listed in the Australian Weeds Committee (2012a) list of Noxious

Weed for Australian States and Territories.

17

Table 2. The number of species that germinated from horse dung based on results from the

15 studies, their weed status globally, in North America and in Australia, their growth form

and life-history characteristics.

Category Total

Total species 249

Weed status internationally

Weed 246

Environmental weed 48

Invasive 118

Invasive/noxious in North America 105

Weed status in Australia

Invasive 3

Naturalized 156

Noxious 16

Native naturalized out of range 9

Growth form

Graminoids 82

Forbs 157

Tree 6

Shrubs 4

Life history

Annual 80

Annual/biennial 13

Annual/perennial 12

Biennial 6

Biennial/perennial 4

Perennial 134