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Journal ArticleDOI

Ingestion by an invasive parakeet species reduces germination success of invasive alien plants relative to ingestion by indigenous turaco species in South Africa

30 Jun 2015-Biological Invasions (Springer International Publishing)-Vol. 17, Iss: 10, pp 3029-3039
TL;DR: The results suggest that Knysna and purple-crested turacos are legitimate seed dispersers of fleshy-fruited invasive plants, while rose-ringed parakeets are mainly seed predators.
Abstract: Avian frugivores play a key role in seed dispersal of many plant species, including invasive alien plants. We assessed the effect of gut passage on the germination of selected invasive alien plant species in South Africa. Fruits of four fleshly-fruited invasive alien plant species: Solanum mauritianum, Cinnamomum camphora, Psidium guajava, and Morus alba, were fed to two species of indigenous turacos, Knysna (Tauraco corythaix) and purple-crested (Gallirex porphyreolophus) turacos, and to invasive rose-ringed parakeets (Psittacula krameri). Seed retention time was determined as this can influence both seed dispersal and germination success. Germination success of ingested seeds was compared with that of manually de-pulped seeds, as well as to seeds in whole fruit. The germination success of seeds of all the invasive plant species increased significantly after ingestion by both turaco species compared with seeds from whole fruits. Germination success of manually de-pulped seeds did not differ significantly from that of turaco ingested seeds. In contrast, seed passage through the digestive tract of rose-ringed parakeets significantly reduced germination success and viability of ingested invasive plant species. Our results suggest that Knysna and purple-crested turacos are legitimate seed dispersers of fleshy-fruited invasive plants, while rose-ringed parakeets are mainly seed predators. Although seed predation by rose-ringed parakeets negatively affects the reproductive success of these plants, it is unlikely that this will suppress the spread of these invasive alien plants in South Africa as they are already well established. Furthermore, they can facilitate dispersal by seed regurgitation and dropping uneaten fruits away from the parent plant. Similar trends could be expected for indigenous seeds that rose-ringed parakeets feed on and therefore these birds remain a negative influence within invaded ecosystems.

Summary (3 min read)

Introduction

  • The process of seed dispersal by avian frugivores usually involves the consumption of pulp and regurgitation or excretion of intact seeds (D'Avila et al.
  • Many studies show that germination is more successful after seeds pass through the digestive tract of frugivores (Traveset 1998; Yagihashi et al.
  • The role of invasive birds as seed dispersers or predators has received little attention, especially in terms of their effect on the dispersal and germination success of invasive plants in South Africa.

Maintenance of study animals

  • Ten captive-bred rose-ringed parakeets, eight captivebred Knysna turacos and two captive-bred purplecrested turacos were housed in outside aviaries (1 9 2.12 9 2.66 m) at the University of KwaZulu-Natal (UKZN), Pietermaritzburg animal house before the experiments were conducted.
  • Birds were fed a mixed fruit maintenance diet daily which consisted of pears, apples, bananas and oranges.
  • All fruits were either grated or chopped and AviPlus Softbill/Mynah pellets and crumble (Avi-products, Durban, South Africa) were added to supplement the maintenance diets.
  • Rose-ringed parakeets were also fed sunflower seeds daily.

Study species

  • Purple-crested and Knysna turacos are medium-sized (c. 300 and 310 g respectively) frugivorous bird species indigenous to South Africa (Sinclair and Ryan 2003) .
  • The rose-ringed parakeet (c. 120 g) is the most introduced parrot species in the world and has established feral populations in many countries, including South Africa (Butler 2003; Sinclair and Ryan 2003; Brooke 1997; Hart and Downs 2014) .
  • Rose-ringed parakeets are native to southern Asia and sub-Saharan Africa (Brooke 1997; Butler 2003) .
  • These frugivorous bird species were selected as Turacos and rose-ringed parakeets eat fruits of both invasive and indigenous plants and co-occur in KwaZulu-Natal, South Africa.
  • Little is known about their effect on the dispersal and germination success of invasive plants in South Africa.

Plant species

  • The authors used fruits of four invasive alien plant species, namely bugweed (Solanum mauritianum), camphor (Cinnamomum camphora), guava (Psidium guajava), and mulberry (Morus alba) in this study.
  • All ripened fruits were collected from naturalized plants near UKZN and fruits were used within 48 h of collection.
  • Bugweed is native to Northern Argentina, Southern Brazil, Paraguay and Uruguay but has become a widespread invasive weed in many countries including South Africa (Olckers 1999; Jordaan et al. 2011a ).
  • Ripe fruits are ingested by a number of bird species, and seeds may be either regurgitated or excreted after consumption (Li 2004 ).

Feeding trials

  • Clean plastic trays, the same size as the cage's base, were placed in each cage to facilitate removal of faeces.
  • For two days prior to each experimental day, the authors incorporated the specific experimental fruit species into the maintenance diet.
  • Excreta were collected from the plastic trays at the end of each trial.

Seed retention time

  • The authors determined seed retention time by recording the time when birds first started feeding, to the time when first undigested seeds appeared in excreta.
  • In each retention time trial, a single specific fruit species for the particular trial was presented either whole or cut up to all birds individually.
  • As retention time may vary with fruit type, the authors measured seed retention time in order to determine the potential effect on germination success and potential seed dispersal distance.

Germination trials

  • The authors removed seeds from each individual bird's excreta or regurgitation and planted these in separate trays (265 9 180 9 75 mm) containing potting soil with no additives within 24 h after the feeding experiment.
  • Manually de-pulped seeds and seeds within whole fruit of each species were planted concurrently in the same manner as ingested seeds.
  • All trays were then placed in the shade house and watered daily.
  • Seeds were considered germinated when seedlings first emerged through the soil surface.
  • The number of germinated seeds was recorded daily for 100 days.

Data analysis

  • The cumulative percentage germination was determined for each tree species.
  • Germination periods for each plant species were compared using Kruskal-Wallis ANOVA tests.
  • Kruskal-Wallis ANOVA tests were also used to compare germination success of ingested seeds to manually de-pulped seeds and whole-fruit controls.
  • Tukey tests were performed where significant differences were evident.
  • All statistical analyses were conducted using STATIS-TICA (Statsoft, Tulsa, version 7, USA).

Mean time to seedling emergence

  • The mean time for emergence of seedlings did not vary between avian species for all invasive plant species (Fig. 2 ).
  • M. alba seeds germinated significantly sooner than all species while C. camphora seedlings emerged significantly later than those of other invasive plant species (Fig. 2a, c ).
  • Seeds contained in whole fruit of P. guajava and S. mauritianum showed significantly lower germination rates than ingested and manually de-pulped seeds (Fig. 3b, d ), while seeds contained in whole fruit of C. camphora emerged at approximately the same time with ingested and manually de-pulped seeds (Fig. 3a, c ).

Germination success

  • Seeds ingested by Knysna and purple-crested turacos had higher germination percentages than those ingested by rose-ringed parakeets for all invasive plant species, except those of C. camphora (Table 1 ; Fig. 3 ).
  • There was no significant difference in germination percentage of ingested seeds between Knysna and purple-crested turacos for all plant species tested, and these seeds had similar germination percentages to those from manually de-pulped seeds (Table 1 ; Fig. 3 ).
  • These germination percentages were significantly higher than for whole fruit seeds for all invasive plant species (Table 1 ).
  • In contrast, seeds that passed through the digestive tract of rose-ringed parakeets (i.e. M. alba and P. guajava) had significantly lower germination percentages compared with turaco ingested and manually de-pulped seeds (Table 1 ; Fig. 3a, b ).
  • Furthermore, germination percentages of seeds passed through the digestive tract of this species was significantly lower than seeds from whole fruits (Table 1 ).

Discussion

  • Knysna and purple-crested turacos gut passage positively affected germination success of all plant species used in this study.
  • Since manually depulped seeds germinated equally well as turacoingested seeds for all invasive plant species, positive effects of seed ingestion by these species are mainly through fruit pulp removal, probably because of the removal of germination inhibitors and release of osmotic pressure.
  • Consistent with other studies M. alba (Jordaan et al. 2012) and C. camphora (Panetta 2001 ) seeds greatly benefited from higher germination percentage due to pulp-removal.
  • The negative effect of rose-ringed parakeets on ingested seeds is not new, Lambert (1989) and Janzen (1981) reported that this species inhibits germination strength of ingested seeds probably due to excessive damage to the seeds caused by it digestive acids.

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ORIGINAL PAPER
Ingestion by an invasive parakeet species reduces
germination success of invasive alien plants relative
to ingestion by indigenous turaco species in South Africa
Vuyisile Thabethe
.
Amy-Leigh Wilson
.
Lorinda A. Hart
.
Colleen T. Downs
Received: 24 March 2015 / Accepted: 16 June 2015 / Published online: 30 June 2015
Ó Springer International Publishing Switzerland 2015
Abstract Avian frugivores play a key role in seed
dispersal of many plant species, including invasive
alien plants. We assessed the effect of gut passage on
the germination of selected invasive alien plant
species in South Africa. Fruits of four fleshly-fruited
invasive alien plant species: Solanum maur itianum,
Cinnamomum camphora, Psidium guajava, and Morus
alba, were fed to two species of indigenous turacos,
Knysna (Tauraco corythaix) and purple-crested (Gal-
lirex porphyreolophus) turacos, and to invasive rose-
ringed parakeets (Psittacula krameri). Seed retention
time was determined as this can influence both seed
dispersal and germination success. Germination suc-
cess of ingested seeds was compared with that of
manually de-pulped seeds, as well as to seeds in whole
fruit. The germination success of seeds of all the
invasive plant species increased significantly after
ingestion by both turaco species compared with seeds
from whole fruits. Germination success of manually
de-pulped seeds did not differ significantly from that
of turaco ingested seeds. In contrast, seed passage
through the digestive tract of rose-ringed parakeets
significantly reduced germination success and viabil-
ity of ingested invasive plant species. Our results
suggest that Knysna and purple-crested turacos are
legitimate seed dispersers of fleshy-fruited invasive
plants, while rose-ringed parakeets are mainly seed
predators. Although seed predation by rose-ringed
parakeets negatively affects the reproductive success
of these plants, it is unlikely that this will suppress the
spread of these invasive alien plants in South Africa as
they are already well established. Furthermore, they
can facilitate dispersal by seed regurgitation and
dropping uneaten fruits away from the parent plant.
Similar trends could be expected for indigenous seeds
that rose-ringed parakeets feed on and therefore these
birds remain a negative influence within invaded
ecosystems.
Keywords Avian frugivore Pulp removal Seed
predation Seed germination Seed retention time
Introduction
Avian frugivores play a key role in seed dispersal of
many plant species worldwide (Cain et al. 2000;
Renne et al. 2000; Vivian-Smith and Gosper 2010;
Jordaan et al. 2011a; Mokotjomela et al. 2013b, 2015).
The process of seed dispersal by avian frugivores
usually involves the consumption of pulp and regur-
gitation or excretion of intact seeds (D’Avila et al.
2010; Fedriani et al. 2011; Czarnecka et al. 2012). This
process is mutually beneficial as plants benefit from
V. Thabethe A.-L. Wilson L. A. Hart
C. T. Downs (&)
DST-NRF Centre for Invasion Biology, School of Life
Sciences, University of KwaZulu-Natal,
Private Bag X01, Scottsville 3209, South Africa
e-mail: downs@ukzn.ac.za
123
Biol Invasions (2015) 17:3029–3039
DOI 10.1007/s10530-015-0932-1

seed dispersal away from the parent plant to locations
with fewer pathogens (Wenny 2001; Aslan 2011;
Fricke et al. 2013) while frugivores benefit from
important food resources and energy rewards (Jordaan
et al. 2011b; Mokotjomela et al. 2013a). Avian
frugivores consume both native and invasive fruit
and therefore can facilitate the rapid spread of fruiting
invasive species (Davis 2011; Mokotjomela et al.
2013b).
Ingestion by frugivores may increase, decrease, or
have no effect on seed germination success of different
plant species (Samuels and Levey 2005; Jordaan et al.
2012; Spotswood et al. 2012; Wilson and Downs
2012; Lessa et al. 2013). Many studies show that
germination is more successful after seeds pass
through the digestive tract of frugivores (Traveset
1998; Yagihashi et al. 1999; Traveset et al. 2001;
Paulsen and Hogstedt 2002; LaFleur et al. 2009;
D’Avila et al. 2010; Reid and Armesto 2011; Jordaan
et al. 2011a). Seed ingestion by dispersers helps seeds
escape predation, competition, and fungal attack under
the parent tree, thereby increasing the chance of
survival (Chimera and Drake 2010; Fedriani et al.
2011; Jordaan et al. 2011a). The chemical or mechan-
ical modification of the seed coat structure due to
ingestion has also been suggested to enhance germi-
nation (Wilson and Downs 2012).
Some studies have also found that seeds ingested by
frugivores may lose viability and thus reduce germi-
nation or have no effect on germination success at all
(LaRosa et al. 1985; Wilson and Downs 2012). This
may be due to excessive abrasion of seeds or the
toxicity and hydrophobic nature of excreta (Vivian-
Smith and Gosper 2010; Reid and Armesto 2011). The
germination response of ingested seeds can be influ-
enced by several factors (Charalambidou et al. 2003).
These include seed retention time, seed coat structure
and seed sizes (Greenberg et al. 2001; Guix 2007).
Seed retention time in frugivores’ guts is the most
important factor for some species in determining their
germination success (Traveset 1998; Cain et al. 2000).
Small seeds tend to have longer retention times and are
less likely to be damaged during gut passage compared
with large seeds (Charalambidou et al. 2003). How-
ever, in some species shorter transit times are observed
and these fruits are preferred by avian frugivores
(Wilson and Downs 2011).
The consumption of fruits by birds may not
necessarily result in successful dispersal (Mandon-
Dalger et al. 2004; Westerman et al. 2006; Combs
et al. 2011). This is because some frugivorous birds are
seed predators (Jordano 1983). Seed predators usually
crush the seeds during feeding and then excrete them
damaged (Jordano 1983). However, some seed preda-
tors may contribute to the dispersal of invasive plants
(Vila and Gimeno 2003). This occurs when predators
do not consume the fruit immediately but carry them
away to feeding roosts for later consumption where
seeds are regurgitated or dropped (Carrion-Tacuri
et al. 2012). This brings the regurgitated seeds into
contact with the soil and forms seed banks that can
successfully germinate, especially when the parental
plants are removed (Witkowski and Garner 2008). It
has been found that some seed predators such as
parrots and Darwin’s finches act as dispersers of native
and invasive alien plants in Hawaii across both short
and long distances (Jordano 1983; Carrion-Tacuri
et al. 2012). However, few studies have been con-
ducted that examine the possible role that seed
predators play in the successful invasion or invasion
suppression of invasive plants globally (Carrion-
Tacuri et al. 2012).
South Africa is one of the countries that have been
extensively invaded by fleshly-fruited invasive plants
(Henderson 2001; van Wilgen et al. 2001; Nel et al.
2004; Richardson and van Wilgen 2004). Many
studies have shown that these plants are consumed
and dispersed by both invasive and indigenous birds
(Jordaan et al. 2011a; Westcott and Fletcher 2011;
Wilson and Downs 2012; Mokotjomela et al. 2013c).
However, the role of invasive birds as seed dispersers
or predators has received little attention, especially in
terms of their effect on the dispersal and germination
success of invasive plants in South Africa. Under-
standing the ecological principles underlying the
invasive process such as how they are dispersed, as
well as what influences their rapid growth, is crucial
for the development of effective and viable manage-
ment strategies to reduce the rate of spread of these
species and for any control measures to be successful.
To date, few studies have looked at the interaction
between invasive bird species, indigenous bird species
and invasive alien plant species, particularly in South
Africa (Jordaan et al. 2011a). Therefore, our aim was
to determine the effects of invasive rose-ringed
parakeets (Psittacula krameri) and indigenous Knysna
(Tauraco corythaix) and purple-crested (Gallirex
porphyreolophus) turacos on seed germination of four
3030 V. Thabethe et al.
123

invasive alien plant species in South Africa. To
investigate this, we compared the germination success
(percentage and rate) of ingested seeds (those that
have passed through the digestive tract or were
regurgitated), manually de-pulped seeds and seeds
within whole fruits. We predicted that fruit processing
by these avian species would increase the germination
success of invasive alien seeds. Results from this study
may play a significant role in the implementation of
effective management strategies of invasive plants in
South Africa and worldwide.
Methods
Maintenance of study animals
Ten captive-bred rose-ringed parakeets, eight captive-
bred Knysna turacos and two captive-bred purple-
crested turacos were housed in outside aviaries
(1 9 2.12 9 2.66 m) at the University of KwaZulu-
Natal (UKZN), Pietermaritzburg animal house before
the experiments were conducted. Birds were fed a
mixed fruit maintenance diet daily which consisted of
pears, apples, bananas and oranges. All fruits were
either grated or chopped and AviPlus Softbill/Mynah
pellets and crumble (Avi-products, Durban, South
Africa) were added to supplement the maintenance
diets. Rose-ringed parakeets were also fed sunflower
seeds daily. Water was provided ad libitum.
Study species
Purple-crested and Knysna turacos are medium-sized
(c. 300 and 310 g respectively) frugivorous bird species
indigenous to South Africa (Sinclair and Ryan 2003).
The rose-ringed parakeet (c. 120 g) is the most
introduced parrot species in the world and has estab-
lished feral populations in many countries, including
South Africa (Butler 2003; Sinclair and Ryan 2003;
Brooke 1997;HartandDowns2014). Rose-ringed
parakeets are native to southern Asia and sub-Saharan
Africa (Brooke 1997;Butler2003). These frugivorous
bird species were selected as Turacos and rose-ringed
parakeets eat fruits of both invasive and indigenous
plants and co-occur in KwaZulu-Natal, South Africa.
Little is known about their effect on the dispersal and
germination success of invasive plants in South Africa.
Plant species
We used fruits of four invasive alien plant species,
namely bugweed (Solanum mauritianum), camphor
(Cinnamomum camphora), guava (Psidium guajava),
and mulberry (Morus alba) in this study. These fruit
species had been observed to be eaten by birds or were
reported as a food source to frugivorous birds in the
wild. All ripened fruits were collected from natural-
ized plants near UKZN and fruits were used within
48 h of collection.
Bugweed is a shrub that usually grows up to 4 m in
height and produces numerous round yellow berries
1–1.5 cm in diameter (Olckers 1999; Jordaan et al.
2011a). Each fruit contains c. 200 seeds that are
0.15–0.20 cm long (Jordaan et al. 2011a). Bugweed is
native to Northern Argentina, Southern Brazil, Para-
guay and Uruguay but has become a widespread
invasive weed in many countries including South
Africa (Olckers 1999; Jordaan et al. 2011a). The great
invasive success of bugweed is facilitated by sec-
ondary distribution of the plant via seed dispersal by
frugivorous animals (Olckers 1999; Henderson 2001).
Camphor is an evergreen tree growing up to 40 m
high (Panetta 2001). This tree produces large quanti-
ties of dark blue to black fleshly fruits approximately
1–1.5 cm in diameter (Panetta 2001). Each fruit
contains a single seed that is 0.75 cm in diameter
(Jordaan et al. 2011a). Over 100,000 fruits can be
produced on a mature tree (Panetta 2001). Ripe fruits
are ingested by a number of bird species, and seeds
may be either regurgitated or excreted after consump-
tion (Li 2004). This species is native to Japan, China
and eastern Asia but has become widely naturalised in
many countries around the world (Panetta 2001).
Guava is a fast growing evergreen tree or shrub
adapted to a wide range of environmental conditions
(Henderson 2001). Guava trees produce yellow,
rounded fruits 3–10 cm in diameter (Henderson
2001). Each fruit contains numerous seeds (c.
100–500) that are 0.3–0.5 cm in diameter (Jordaan
et al. 2011a). This species is native to Central
America (Berens et al. 2008).
Mulberry is a deciduous tree growing up to 15 m in
height with juicy elongated purple-black fruits (Hen-
derson 2001). The fruits are 2–3 cm long and each
fruit contains up to c. 30 seeds (Henderson 2001). The
mulberry is native to eastern United States and has
Indigenous turaco species in South Africa 3031
123

been widely introduced globally for its sweet and
edible fruits (Henderson 2001).
Feeding trials
We moved birds to a constant environment room with
a 12L:12D photoperiod at 25 ± 1 °C two weeks
before trials were conducted and housed them indi-
vidually in cages (42.7 9 43 9 59.3 cm). Clean
plastic trays, the same size as the cage’s base, were
placed in each cage to facilitate removal of faeces.
For two days prior to each experimental day, we
incorporated the specific experimental fruit species
into the maintenance diet. On the experimental day,
we fed birds a diet of only each specific invasive alien
fruit species, either whole or cut up. Each trial was run
for 12 h (from 06h00–18h00). Fruits were weighed to
0.01 g before and after each trial to determine the
amount of fruit eaten. Birds were also weighed to 0.5 g
30 min prior to, and again at the end, of each trial.
Control fruits were placed in the experimental room
and were also weighed prior to, and at the end, of each
trial to control for evaporative water loss. Excreta
were collected from the plastic trays at the end of each
trial. A minimum of 3 days was left between each trial
depending on fruit availability. The maintenance diet
was fed between each trial to enable birds to regain
any body mass lost during experiments.
Seed retention time
We determined seed retention time by recording the
time when birds first started feeding, to the time when
first undigested seeds appeared in excreta. For regur-
gitated seeds, the seed retention time was measured as
the time when birds first fed to the time when
undamaged seeds appeared in the regurgitated food.
Seed retention time was measured on the experimental
day only. In each retention time trial, a single specific
fruit species for the particular trial was presented
either whole or cut up to all birds individually.
Previous studies have reported that the maximum gut
retention time for turacos is ca. 12–35 min (Wilson
and Downs 2012) while that of parakeets is ca.
30–50 min (Koutsos et al. 2001). As retention time
may vary with fruit type, we measured seed retention
time in order to determine the potential effect on
germination success and potential seed dispersal
distance.
Germination trials
We removed seeds from each individual bird’s
excreta or regurgitation and planted these in separate
trays (265 9 180 9 75 mm) containing potting soil
with no additives within 24 h after the feeding
experiment. Seeds were covered with a soil layer c.
0.5 cm deep. Manually de-pulped seeds and seeds
within whole fruit of each species were planted
concurrently in the same manner as ingested seeds.
All trays were then placed in the shade house and
watered daily. Seeds were considered germinated
when seedlings first emerged through the soil surface.
The number of germinated seeds was recorded daily
for 100 days. The date of seedling emergence was
recorded and once counted, seedlings were removed
from the tray.
Data analysis
The cumulative percentage germination was deter-
mined for each tree species. Mean cumulative germi-
nation percentage was calculated for ingested, pulp
manually removed and whole fruits seeds for each fruit
species. Germination periods for each plant species
were compared using Kruskal–Wallis ANOVA tests.
Seed retention time for each individual bird and for a
specific fruit was also analyzed using Kruskal–Wallis
ANOVA tests. Kruskal–Wallis ANOVA tests were also
used to compare germination success of ingested seeds
to manually de-pulped seeds and whole-fruit controls.
Further investigations with post hoc Tukey tests were
performed where significant differences were evident.
All statistical analyses were conducted using STATIS-
TICA (Statsoft, Tulsa, version 7, USA).
Results
Seed retention time
Seed retention time did not vary significantly between
Knysna and purple-crested turacos but varied signifi-
cantly between rose-ringed parakeets and both species
of turacos for most invasive plant species (Fig. 1).
Knysna and purple-crested turacos had shorter retention
times (10–22 and 12–19 min respectively) when fed
M. alba seeds than rose-ringed parakeets (31–46 min,
3032 V. Thabethe et al.
123

Kruskal–Wallis ANOVA H
2
= 14.36, n = 20,
P = 0.001, Fig. 1a). Similarly, both turaco species
had significantly shorter seed retention times
(17–31 min and 20–21 min respectively) than rose-
ringed parakeets (34–50 min) when fed P. guajava fruit
(Kruskal–Wallis ANOVA H
2
= 14.36, n = 20,
P = 0.001 (Fig. 1b). Retention times for C. camphora
seeds did not vary significantly between purple-crested
turacos and rose-ringed parakeets (post hoc Tukey,
P = 0.14, Fig. 1c) but varied significantly between
Knysna turacos and rose-ringed parakeets (post hoc
Tukey, P = 0.009, Fig. 1c) (Kruskal–Wallis ANOVA
H
2
= 9.39, n = 15, P = 0.009, Fig. 1c). Seed reten-
tion time did not differ significantly between Knysna
and purple-crested turacos when fed S. mauritianum
fruits (Kruskal–Wallis ANOVA H
1
= 0.068, n = 10,
P = 0.79, Fig. 1d). Rose-ringed parakeets regurgitated
C. camphora seed; excreted few M. alba and P. guajava
seeds but did not ingest S. mauritianum seeds at all.
Mean time to seedling emergence
The mean time for emergence of seedlings did not vary
between avian species for all invasive plant species
(Fig. 2). However, seedling emergence from ingested
seeds varied significantly among the invasive plant
species (Kruskal–Wallis ANOVA H
3
= 70.57,
n = 174, P = 0.00, Fig. 2). M. alba seeds germinated
significantly sooner than all species while C. camphora
seedlings emerged significantly later than those of other
invasive plant species (Fig. 2a, c). All M. alba ingested
by avian species germinated after ca. 5 days (Fig. 2a),
which was not significantly earlier than manually de-
pulped seeds but significantly sooner than whole fruit
seeds (Kruskal–Wallis ANOVA H
4
= 22.84, n = 38,
P = 0.00, Fig. 3a). Ingested S. mauritianum seeds
started germinating after ca. 13 days (Fig. 2d); this was
not significantly earlier than manually de-pulped seeds
(Fig. 3d) but significantly sooner than whole fruit seeds,
0
10
20
30
40
50
60
70
Knysna turaco Purple-crested turaco Rose-ringed parakeet
Knysna turaco Purple-crested turaco Knysna turaco Purple-crested turacoRose-ringed parakeet
Species
0
10
20
30
40
50
60
70
Seed retention time (min)Seed retention time (min)
Knysna turaco Purple-crested turaco Rose-ringed parakeet
Species
Species Species
0
10
20
30
40
50
60
70
Seed retention time (min)
0
10
20
30
40
50
60
70
Seed retention time (min)
(a) (c)
(b) (d)
Fig. 1 Seed retention time for three avian species feeding on fruits of a M. alba, b P. guajava, c C. camphora, and d S. mauritianum,
where boxes are 25 and 75 % quartiles, the solid black squares within the boxes the medians, bars show 10 and 90 % values
Indigenous turaco species in South Africa 3033
123

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01 Jan 2005
TL;DR: In this paper, the authors compared the fruit fates of C. orbiculatus and native American holly (Ilex opaca) and examined the influence of seed treatment and light intensity on seed germination and seed growth.
Abstract: Oriental bittersweet (Celastrus orbiculatus Thunb.) is a non-indigenous, invasive woody vine in North America that proliferates in disturbed open sites. Unlike most invasive species, C. orbiculatus exhibits a ‘sit and wait’ strategy by establishing and persisting indefinitely in undisturbed, closed canopy forest and responding to canopy disturbance with rapid growth, often overtopping trees. We compared fruit fates of C. orbiculatus and native American holly (Ilex opaca). We also explored mechanisms for this ‘sit and wait’ invasion strategy by testing the effect of C. orbiculatus fruit crop density on removal rates and by examining the influence of seed treatment and light intensity on seed germination and seedling growth. More C. orbiculatus than I. opaca fruits became damaged, and damage occurred earlier. More fruit fell from C. orbiculatus than I. opaca, but removal rates by frugivores did not differ (76.0 ± 4.2% vs 87.5 ± 3.7%, respectively). Density (number of fruits in a patch) of C. orbiculatus did not influence removal rates. Scarification (bird-ingestion) of C. orbiculatus seed delayed germination but seeds germinated in similar proportion to manually defleshed seeds (sown either singly or all seeds from a fruit). Germination of seeds within intact fruits was inhibited and delayed compared to other treatments. Seed treatment did not affect seedling growth. The proportion of seeds germinating and time until germination was similar among five light intensity levels, ranging from full sun to closed-canopy. Seedlings in >70% photosynthetically active radiation (PAR) had more leaves, heavier shoots, and longer, heavier roots than seedlings at lower PAR levels. Results show that most (>75%) C. orbiculatus seeds are dispersed, seedlings can establish in dense shade, and plants grow rapidly when exposed to high light conditions. Control strategies for this highly invasive species should likely focus on minimizing seed dispersal by vertebrates.

90 citations

Journal ArticleDOI
22 Feb 2016-PeerJ
TL;DR: Internal dispersal was investigated by searching for seeds in faeces opportunistically collected at communal roosts, foraging sites and nests of eleven parrot species in different habitats and biomes in the Neotropics, suggesting the importance of parrots as endozoochorous dispersers has been largely under-appreciated.
Abstract: Despite the fact that parrots (Psitacifformes) are generalist apex frugivores, they have largely been considered plant antagonists and thus neglected as seed dispersers of their food plants. Internal dispersal was investigated by searching for seeds in faeces opportunistically collected at communal roosts, foraging sites and nests of eleven parrot species in different habitats and biomes in the Neotropics. Multiple intact seeds of seven plant species of five families were found in a variable proportion of faeces from four parrot species. The mean number of seeds of each plant species per dropping ranged between one and about sixty, with a maximum of almost five hundred seeds from the cacti Pilosocereus pachycladus in a single dropping of Lear’s Macaw (Anodorhynchus leari). All seeds retrieved were small (<3 mm) and corresponded to herbs and relatively large, multiple-seeded fleshy berries and infrutescences from shrubs, trees and columnar cacti, often also dispersed by stomatochory. An overview of the potential constraints driving seed dispersal suggest that, despite the obvious size difference between seeds dispersed by endozoochory and stomatochory, there is no clear difference in fruit size depending on the dispersal mode. Regardless of the enhanced or limited germination capability after gut transit, a relatively large proportion of cacti seeds frequently found in the faeces of two parrot species were viable according to the tetrazolium test and germination experiments. The conservative results of our exploratory sampling and a literature review clearly indicate that the importance of parrots as endozoochorous dispersers has been largely under-appreciated due to the lack of research systematically searching for seeds in their faeces. We encourage the evaluation of seed dispersal and other mutualistic interactions mediated by parrots before their generalized population declines contribute to the collapse of key ecosystem processes.

53 citations


Cites result from "Ingestion by an invasive parakeet s..."

  • ...Our review of the literature showed that intact seeds of other plant families have been retrieved from parrot faeces, including Mutingiaceae, Dilleniaceae, Myrtaceae, Araliaceae, Coriariaceae, Elaeocarpaceae, Ericaceae, Podocarpaceae, Polygonaceae, Rubiaceae and Lauraceae (Fleming et al., 1985; Oliveira, Nunes & Farias, 2012; Young, Kelly & Nelson, 2012; Thabethe et al., 2015)....

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  • ...In any case, our exploratory experiments and findings add to those of previous studies suggesting that parrots can be endozoochorous dispersers enhancing or limiting seed germinability to variable extents depending on plant and parrot species (Fleming et al., 1985; Oliveira, Nunes & Farias, 2012; Thabethe et al., 2015), as stated for recognized avian seed dispersers (Traveset, Robertson & Rodríguez-Pérez, 2007)....

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  • ...aceae, Myrtaceae, Araliaceae, Coriariaceae, Elaeocarpaceae, Ericaceae, Podocarpaceae, Polygonaceae, Rubiaceae and Lauraceae (Fleming et al., 1985; Oliveira, Nunes & Farias, 2012; Young, Kelly & Nelson, 2012; Thabethe et al., 2015)....

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Journal ArticleDOI
02 Jan 2018
TL;DR: Parrots (Psittaciformes) have been viewed as efficient consumers of the reproductive structures of plants and have been excluded from studies focusing on plant-animal mutualistic relations.
Abstract: Parrots (Psittaciformes) have been viewed as efficient consumers of the reproductive structures of plants. Consequently, parrots have been excluded from studies focusing on plant–animal mutualistic...

38 citations

Book ChapterDOI
01 Jan 2020
TL;DR: It is argued that many invasions in South Africa are promising candidates for testing hypotheses related to species interactions and invasiveness, and how these depend on the eco-evolutionary experience of the alien species.
Abstract: Ecological interactions, especially those that are beneficial (i.e. mutualism) or detrimental (i.e. parasitism), play important roles during the establishment and spread of alien species. This chapter explores the role of these interactions during biological invasions in South Africa, covering a wide range of taxonomic groups and interaction types. We first discuss the different ways in which interactions can be reassembled following the introduction of alien species, and how these depend on the eco-evolutionary experience of the alien species. We then discuss documented examples of parasitism and mutualism associated with invasions in South Africa and how these relate to various ecological and evolutionary hypotheses aimed at explaining species invasiveness. Selected examples of how invasive species impact on native species interactions are provided. A diverse array of biotic interactions (e.g. pollination, fish and mollusc parasitism, plant-soil mutualistic bacteria, seed dispersal) have been studied for various invasive species in South Africa. Surprisingly, only a few of these studies explicitly tested any of the major hypotheses that invoke biotic interactions and are commonly tested in invasion ecology. We argue that many invasions in South Africa are promising candidates for testing hypotheses related to species interactions and invasiveness.

36 citations


Cites background from "Ingestion by an invasive parakeet s..."

  • ...…fruits of invasive species over those produced by native species by birds is that some invasive species offer higher nutritional rewards (e.g. Cinnamomum camphora, Lantana camara, Morus alba, Psidium guajava, Solanum mauritianum; Jordaan et al. 2011; Mokotjomela et al. 2013a; Thabethe et al. 2015)....

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  • ...We know of one example from South Africa, where invasive Rose-ringed Parakeets, Psittacula krameri, may impede establishment of alien plants due to reduced germination of ingested seeds (Thabethe et al. 2015)....

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  • ...Another factor promoting the preference of fruits of invasive species over those produced by native species by birds is that some invasive species offer higher nutritional rewards (e.g. Cinnamomum camphora, Lantana camara, Morus alba, Psidium guajava, Solanum mauritianum; Jordaan et al. 2011; Mokotjomela et al. 2013a; Thabethe et al. 2015)....

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  • ...Psittacula krameri, may impede establishment of alien plants due to reduced germination of ingested seeds (Thabethe et al. 2015)....

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  • ...Indeed, native frugivorous species are often responsible for the increased invasiveness of many alien plants in South Africa (Jordaan et al. 2011; Wilson and Downs 2012; Thabethe et al. 2015; Mokotjomela et al. 2016)....

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References
More filters
Journal ArticleDOI
TL;DR: These comparative studies provide insights into the more general question “Do alien invasive plants usually outperform co-occurring native species, and to what degree does the answer depend on growing conditions?”
Abstract: ▪ Abstract In the search to identify factors that make some plant species troublesome invaders, many studies have compared various measures of native and alien invasive plant performance. These comparative studies provide insights into the more general question “Do alien invasive plants usually outperform co-occurring native species, and to what degree does the answer depend on growing conditions?” Based on 79 independent native-invasive plant comparisons, the alien invaders were not statistically more likely to have higher growth rates, competitive ability, or fecundity. Rather, the relative performance of invaders and co-occurring natives often depended on growing conditions. In 94% of 55 comparisons involving more than one growing condition, the native's performance was equal or superior to that of the invader, at least for some key performance measures in some growing conditions. Most commonly, these conditions involved reduced resources (nutrients, light, water) and/or specific disturbance regimes. I...

1,271 citations


"Ingestion by an invasive parakeet s..." refers background in this paper

  • ...The seeds of many other invasive plant species have also been shown to benefit from ingestion by birds (Daehler 2003; Corlett 2005; Bartuszevige and Gorchov 2006; Chimera and Drake 2010; Aslan 2011; Combs et al. 2011; Carrion-Tacuri et al. 2012; Czarnecka et al. 2012)....

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Journal ArticleDOI
TL;DR: It is argued that genetic methods provide a broadly applicable way to monitor long-distance seed dispersal and, hence, that better data is needed from the tails of seeds that travel long distances.
Abstract: Long-distance seed dispersal influences many key aspects of the biology of plants, including spread of invasive species, metapopulation dynamics, and diversity and dynamics in plant communities. However, because long-distance seed dispersal is inherently hard to measure, there are few data sets that characterize the tails of seed dispersal curves. This paper is structured around two lines of argument. First, we argue that long-distance seed dispersal is of critical importance and, hence, that we must collect better data from the tails of seed dispersal curves. To make the case for the importance of long-distance seed dispersal, we review existing data and models of long-distance seed dispersal, focusing on situations in which seeds that travel long distances have a critical impact (colonization of islands, Holocene migrations, response to global change, metapopulation biology). Second, we argue that genetic methods provide a broadly applicable way to monitor long-distance seed dispersal; to place this argument in context, we review genetic estimates of plant migration rates. At present, several promising genetic approaches for estimating long-distance seed dispersal are under active development, including assignment methods, likelihood methods, genealogical methods, and genealogical/demographic methods. We close the paper by discussing important but as yet largely unexplored areas for future research.

1,121 citations


"Ingestion by an invasive parakeet s..." refers background in this paper

  • ...Avian frugivores play a key role in seed dispersal of many plant species worldwide (Cain et al. 2000; Renne et al. 2000; Vivian-Smith and Gosper 2010; Jordaan et al. 2011a; Mokotjomela et al. 2013b, 2015)....

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  • ...Seed retention time in frugivores’ guts is the most important factor for some species in determining their germination success (Traveset 1998; Cain et al. 2000)....

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  • ...important factor for some species in determining their germination success (Traveset 1998; Cain et al. 2000)....

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Journal ArticleDOI
TL;DR: The hypothesis that enhanced germination may be more advantageous in unpredictable or less constant environments is supported.
Abstract: The capacity of seeds to germinate after ingestion by frugivores is important for the population dynamics of some plant species and significant for the evolution of plant-frugivore interactions. In this paper the effects of different vertebrates on seed germination of nearly 200 plant species are reviewed, searching for patterns that predict the circumstances in which germination of seeds is enhanced, inhibited, or unaffected by the passage through the digestive tract of a seed disperser. It was found that seed dispersers commonly have an effect on the germinability of seeds, or on the rate of germination, or both, in about 50% of the plants they consume, although the diversity of animal species tested so far is still rather low (42 bird species, 28 non-flying mammals, 10–15 bats, 12 reptiles, 2 fishes). Enhancement of germination occurred about twice as often as inhibition. In spite of the morphological and physiological differences in their digestive tracts, the different animal groups tested have similar effects on seed germination, although non-flying mammals tend to influence germination slightly more often than the other groups. Data on fishes are still too scarce for any generalization. Seed retention time in the dispersers' digestive tract is one factor affecting germination, and helps to explain the variation in seed responses observed among plant species, and even within a species. However other factors are also important; for example, the type of food ingested along with the fruits may affect germination through its influence on chemical or mechanical abrasion of the seed coat. Seed traits such as coat structure or thickness may themselves be responsible for some of the variation in seed retention times. Seeds of different sizes, which usually have different transit times through frugivores, and seeds of either fleshy or dry fruits, show often similar germination response to gut passage. Seeds of different plants species differ strongly in their germination response after ingestion, even by the same frugivore species. Congeneric plants often show little consistency in their response. Even within a species variation is found which can be related to factors such as the environmental conditions under which germination takes place, seed morphology, seed age, and the season when the seeds are produced. The effect of gut passage on germination differs between tropical and temperate zones. Seed germination of both shrubs and trees (data on herbaceous species are still scarce) in the temperate zone is more frequently enhanced than in the tropics. This result supports the hypothesis that enhanced germination may be more advantageous in unpredictable or less constant environments. Significant differences in frugivore-mediated germination are also found among different life forms. In both tropical and temperate zones, trees appear to be consistently more affected than shrubs or herbs. This might be due to an overall higher thickness of the seed coats, or to a higher frequency of seed-coat dormancy in tree species. The influence of frugivory upon the population dynamics of a species has to be evaluated relative to other factors that influence germination and seedling recruitment at a particular site. Whether seed ingestion by dispersers is really advantageous to a plant (as has commonly been assumed) can only be assessed if we also determine the fate of the ingested seeds under natural conditions, and compare it to the fate of seeds that have not been ingested.

558 citations


"Ingestion by an invasive parakeet s..." refers background in this paper

  • ...Many studies show that germination is more successful after seeds pass through the digestive tract of frugivores (Traveset 1998; Yagihashi et al. 1999; Traveset et al. 2001; Paulsen and Hogstedt 2002; LaFleur et al. 2009; D’Avila et al. 2010; Reid and Armesto 2011; Jordaan et al. 2011a)....

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  • ...Seed retention time in frugivores’ guts is the most important factor for some species in determining their germination success (Traveset 1998; Cain et al. 2000)....

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Journal Article
TL;DR: The ecological evidence for the impacts of invasive alien plants on South African ecosystems is examined and a framework to suggest the main challenges for research is suggested that will address critical gaps in knowledge and that will serve explicit management needs is suggested.
Abstract: .South Africa has a long history of problems with invasive alien species, and of research and management of biological invasions (Table 1). The Working for Water programme 26–28 was started in 1995 to conduct and coordinate alien-plant management throughout South Africa. The programme initially worked only in watersheds and riparian areas, but now leads alien-plant management initiatives in all natural and semi-natural ecosystems. It has grown into one of the world’s biggest programmes dealing with invasive alien species. The enterprise’s success has been attributed to its multi-faceted and cross-disciplinary nature that has enabled it to leverage local and international funding and continuing political support. The programme is driven by multi-disciplinary ecological, hydrological, social and economic goals. In practice it has focused on hydrological and social concerns (as embodied in the name of the programme), and its ecological goals are less clearly defined. The extent to which the aim of improving the ecological integrity of natural ecosystems through the control of invasive alien plants has therefore not always been clear to both programme participants and other stakeholders. In this paper, we examine the ecological evidence for the impacts of invasive alien plants on South African ecosystems. We begin with a brief review of what is known about the extent of invasions and influences of these plants, and then discuss the consequences for the delivery of ecosystem goods and services to people. However, the emerging field of invasion ecology addresses issues beyond the effects of invasive species. The different aspects of invasion ecology can be related to the critical stages of invasion, and these stages also provide a useful framework for classifying the management interventions that are required to deal with the problem (Box 1). Our understanding of many of the broader aspects of invasion ecology needs to improve, and we use this framework to suggest the main challenges for research that will address critical gaps in knowledge and that will serve explicit management needs. Components of impact

504 citations

Journal Article
TL;DR: It is suggested that directed dispersal is more common than previously believed even in the absence of plant adaptations to promote it, and may often be ecologically important if one dispersal vector has a disproportionate effect on plant recruitment.
Abstract: Seed dispersal can be advantageous (1) in escape from density- or distance-dependent seed and seedling mortality, (2) by colonization of suitable sites unpredictable in space and time, and (3) by directed dispersal to particular sites with a relatively high probability of survival. Most previous research on the consequences of seed dispersal has focused on escape and colonization because adaptations ensuring directed dispersal are not expected under the paradigm of diffuse mutualism that characterizes the modern view of seed dispersal evolution. In this paper, I suggest that directed dispersal is more common than previously believed even in the absence of plant adaptations to promote it. Directed dispersal may be seen in particular among animaldispersed plants and in arid ecosystems or successional areas, but has been overlooked due to the lack of detailed data on seed shadows generated by particular species, and the fact that the alternative advantages of dispersal are not mutually exclusive. Although directed dispersal is never thought to be the only advantage of dispersal, it may often be ecologically important if one dispersal vector has a disproportionate effect on plant recruitment. Furthermore, in human-disturbed and managed ecosystems, directed dispersal may be important in restoration. More studies detailing the consequences of different patterns of seed dispersal will be useful for conservation and management strategies.

429 citations


"Ingestion by an invasive parakeet s..." refers background in this paper

  • ...…Bag X01, Scottsville 3209, South Africa e-mail: downs@ukzn.ac.za seed dispersal away from the parent plant to locations with fewer pathogens (Wenny 2001; Aslan 2011; Fricke et al. 2013) while frugivores benefit from important food resources and energy rewards (Jordaan et al. 2011b;…...

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  • ...seed dispersal away from the parent plant to locations with fewer pathogens (Wenny 2001; Aslan 2011; Fricke et al. 2013) while frugivores benefit from important food resources and energy rewards (Jordaan et al....

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