Download Abstract Nutrient enrichment and climate warming effects on plant

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Maria Magdalena Meza-Lopez
2015
Abstract
Nutrient enrichment and climate warming effects on
plant and herbivore invasions in wetland communities
by
Maria Magdalena Meza-Lopez
Ecosystems invaded by one exotic species often contain abundant populations
of other exotic species. This may reflect facilitative exotic species interactions,
common responses to anthropogenic factors (nutrient enrichment and/or climate
warming), or result from common paths of introduction. My dissertation asked 1)
Do exotic species on multiple trophic levels reciprocally facilitate each other’s
invasions of freshwater wetlands in southeast Texas?, 2) Do nutrient enrichment
and/or climate warming increase exotic plant performance in the presence or
absence of exotic herbivores?, 3) Do nutrient enrichment, warming, plant
invasions, and their interactions affect exotic herbivore performance? A factorial
field mesocosm experiment that manipulated the order of exotic plant and exotic
herbivore invasions found no evidence of reciprocal exotic species facilitation
that would lead to an invasional meltdown in native wetland communities invaded
by Pomacea maculata (apple snail) and Alternanthera philoxeroides (alligator
weed). Pomacea maculata may facilitate A. philoxeroides invasions because
they preferentially consumed native plants but P. maculata invasions did not
depend on the presence of A. philoxeroides. Greenhouse experiments showed
that elevated nutrients (nitrogen and phosphorus) had no direct impact on
P. maculata survival and Eichhornia crassipes (water hyacinth) and
A. philoxeroides are not ideal food sources for P. maculata. However,
P. maculata growth increased with elevated nutrients via changes in plants but
was independent of plant identity. In field mesocosm experiments, elevated
nutrients increased plant invasions independent of warming by more strongly
increasing growth of exotic plants. However, warming can influence the
magnitude of nutrient enrichment effects on exotic species. In addition,
P. maculata performance was insensitive to elevated nutrients but warming
increased the reproductive output of P. maculata four-fold. Together these
results suggest that exotic herbivores that have high impacts on native plants
may facilitate plant invasions, that nutrient enrichment and warming may each
increase the performance of exotic herbivores, and plant invasions are more very
sensitive to nutrient enrichment than warming. Furthermore, these studies
suggest that it is critical to investigate the effects of multiple anthropogenic
factors on native and exotic species at the community level.
Acknowledgments
I would like to thank my advisor Evan Siemann for giving me the opportunity to
learn and growth as scientist and for believing in me. Thank you for your patience
and for having the energy to work with me endlessly on many things that
included fellowship applications, experimental design, setting up experiments,
data analysis, and manuscript preparations. I also want to thank you for always
pushing me to exceed limits throughout graduate school. You have made me a
stronger person in many ways and have prepared me for the challenges that lie
ahead. Thank you for all of your help.
I want to thank my committee members Rudolf Volker, Qilin Li, and Anna
Armitage for guidance with experimental designs and for challenging me to think
critically and broadly. In addition, I want to thank Amy Dunham for her support
and guidance as a committee member. Special thanks to Anna Armitage for her
support and for not hesitating to step in when I needed her help.
Thanks to all of the graduate students that welcomed me when I joined the
department, those that joined the department later, and to the Chinese visiting
students in our lab for making graduate school enjoyable. Special thanks to Leiyi
Chen (a.k.a. Jenny) and Ling Zhang for their help in the field and in lab and for
always willing and ready to grab a beer at the end of the day regardless of what
was going on. I also want to give special thanks to Stephen Hovick for his advice
and mentoring during my first year of graduate school, to Chris Roy for being a
good officemate, to my labmates Chris Gabler, Juli Carillo, and Thomas Ye for
v
their advice and useful comments on experimental designs, fellowship
applications, and manuscripts.
I am also very grateful for everyone that provided field and laboratory
assistance throughout the years including lab technicians, graduate and
undergraduate students. Thank you Candice Tiu, Nick Hill, Abby Lamb, Daniel
McDermott, Qiang Yang, Gang Liu, Ariel Nixon, Erica Soltero, Hannah Chen,
Cassandra Corrales, Jordan Bunch, Josh Hwang, Hayden Ju, Peter Sylvers,
Boris Zhong, and Michelle Shapiro. Special thanks to Dana Galvan for
volunteering and assisting me in field and in the lab for three years. I also want to
thank Sarah Margolis who volunteered and provided immense help in the field
during my last field season.
I want to thank my family for motivating me and giving me the drive to
continue and overcome the challenges that I have encountered along the way.
Thanks to my husband William Lopez for his love, patience, advice and support
along this journey. Thank you also for enduring long hot days at South Campus
to assist me with my field experiments. Thanks to my mother and siblings for
their understanding, support, and love along the way. I also want to give a
special shout out to my fur babies Boots and Buddha for their unconditional love,
for keeping me company and assisting me at South Campus.
Thanks to the numerous organizations that have funded me and my work,
including the Environmental Protection Agency, Ford Foundation, Houston
Conchology Society, Society of Wetland Scientist, Kroger, Ecology and
Evolutionary Biology department at Rice University, and Rice University Shell
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Center for Sustainability. I also want to thanks Chef Derrix at Rice University for
providing large quantities of romaine lettuce to sustain apple snail populations in
the lab.
I want to give special thanks to AGEP and Ford Foundation. Thanks Theresa
Chatman and Richard Tapia for your support, advice, and mentoring. I also want
to thank Chris O’Brien for her support, advice, motivations, and for her sincere
friendship. Thanks to all of friends that I have acquired throughout the years
through these programs and organizations. Special thanks to Joseph Young,
Toni Tullius, and Nabor Reyna for their advice, mentoring, and friendship.
I dedicate this work to my nieces Leticia, Crystal, Karen, Vanessa, Daniela,
Gabriela, Jazmin, Wendy (2), Brenda, Dayana, and Alondra, and my nephew
Cesar and grandnephew Landen to encourage them to pursue their dreams and
goals.
vii
Contents
Abstract ............................................................................................................... ii
Acknowledgments ............................................................................................. iv
Contents ............................................................................................................ vii
List of Figures ..................................................................................................... x
List of Tables .................................................................................................... xii
List of Appendix Figures................................................................................. xiii
List of Appendix Tables .................................................................................. xiv
Ch 1 Introduction .............................................................................................. 15
Ch 2 Experimental test of the Invasional Meltdown Hypothesis: an exotic
herbivore facilitates an exotic plant, but the plant does not reciprocally
facilitate the herbivore ..................................................................................... 21
2.1. Abstract .................................................................................................... 21
2.2. Keywords.................................................................................................. 22
2.3. Introduction............................................................................................... 22
2.4. Methods.................................................................................................... 26
2.4.1. Study system ................................................................................ 26
2.4.2. Establishing native wetland communities ..................................... 27
2.4.3. Exotic species............................................................................... 28
2.4.4. Experimental manipulation ........................................................... 28
2.4.5. Data analyses ............................................................................... 29
2.5. Results ..................................................................................................... 30
2.5.1. Reciprocal facilitation between exotic species (IMH) .................... 30
2.5.2. Exotic species impacts ................................................................. 31
2.6. Discussion ................................................................................................ 32
2.6.1. Reciprocal facilitation between exotic species (IMH) .................... 32
2.6.2. Exotic species impacts ................................................................. 34
2.7. Acknowledgments .................................................................................... 35
Ch 3 Nutrient enrichment increased exotic snail Pomacea maculata growth
independent of native and exotic wetland plant identity .............................. 41
3.1. Abstract .................................................................................................... 41
viii
3.2. Keywords.................................................................................................. 42
3.3. Introduction............................................................................................... 43
3.4. Methods.................................................................................................... 46
3.4.1. Study system ................................................................................ 46
3.4.2. Experimental set-up...................................................................... 48
3.4.3. Exp.1: Nutrients’ direct and indirect effects on P. maculata mortality
and shell length ...................................................................................... 48
3.4.4. Exp. 2: Nutrient enrichment effects on P. maculata, plants, and
plant-herbivore interactions .................................................................... 49
3.4.5. Data analyses ............................................................................... 50
3.5. Results ..................................................................................................... 51
3.5.1. Exp. 1: Nutrient enrichment’s direct and indirect effects on
P. maculata mortality and shell length .................................................... 51
3.5.2. Exp. 2: Nutrient enrichment effects on P. maculata, plants, and
plant-herbivore interactions .................................................................... 52
3.6. Discussion ................................................................................................ 52
3.7. Acknowledgments .................................................................................... 57
Ch 4 Nutrient enrichment effects on invasions depend on climate warming:
an experimental test with freshwater wetland plant communities ............... 62
4.1. Abstract .................................................................................................... 62
4.2. Keywords.................................................................................................. 63
4.3. Introduction............................................................................................... 63
4.4. Methods.................................................................................................... 69
4.4.1. Study system ................................................................................ 69
4.4.2. Experimental setup ....................................................................... 70
4.4.3. Data analyses ............................................................................... 72
4.5. Results ..................................................................................................... 73
4.6. Discussion ................................................................................................ 75
4.7. Acknowledgements .................................................................................. 79
Ch 5 Warming increased exotic snail reproduction independent of nutrient
enrichment and plant invasions in wetland communities ............................ 88
5.1. Abstract .................................................................................................... 88
5.2. Keywords.................................................................................................. 89
ix
5.3. Introduction............................................................................................... 89
5.4. Methods.................................................................................................... 92
5.4.1. Study system ................................................................................ 92
5.4.2. Experimental setup ....................................................................... 95
5.4.3. Data analyses ............................................................................... 96
5.5. Results ..................................................................................................... 97
5.5.1. Snails ............................................................................................ 97
5.5.2. Plants ........................................................................................... 98
5.6. Discussion ................................................................................................ 99
5.7. Acknowledgements ................................................................................ 105
References ...................................................................................................... 113
x
List of Figures
Figure 2-1 (a) Alternanthera philoxeroides dry mass and (b) mass as
percent of total plant mass in treatments with exotic plants introduced in
June 2011. Means + 1 SE. Means with the same letter were not significantly
different in post-hoc tests. P = exotic plant, S – P = exotic snail invasion
followed by exotic plant invasion, P & S = simultaneous exotic plant and
exotic snail invasion ........................................................................................ 38
Figure 2-2 (a) Native plant dry mass and (b) diversity in each invasion
treatment. Means + 1 SE. Means with the same letter were not significantly
different in post-hoc tests. C = native plants and native snails, P = exotic
plant, S = exotic snail, P – S = exotic plant invasion followed by exotic snail
invasion, S – P = exotic snail invasion followed by exotic plant invasion, P
& S = simultaneous invasion by exotic plant and exotic snail ..................... 39
Figure 2-3 (a) Pomacea maculata operculum length, (b) adult mass, (c)
reproductive output (total egg volume) and (d) juvenile abundance were
independent of A. philoxeroides invasions when snails were introduced in
June 2011. Means + 1 SE. S = exotic snail, P – S = exotic plant invasion
followed by exotic snail invasion, P & S = simultaneous invasion by exotic
plant and exotic snail ....................................................................................... 40
Figure 3-1 The dependence of exotic P. maculata (a) shell length on
nutrients and plants and (b) percent mortality on plant species in
experiment 1. Means+1SE. Means with the same letter were not
significantly different in post-hoc tests. E. c. = E. crassipes and A. p. = A.
philoxeroides .................................................................................................... 59
Figure 3-2 The dependence of exotic P. maculata operculum length on (a)
nutrients and (b) plants in experiment 2. Means +1SE. Means with the same
letters were not significantly different in post-hoc tests. L. s. = L. spongia,
H. u. = H. umbellata, A. p. = A. philoxeroides, E. c. = E. crassipes .............. 60
Figure 3-3 The dependence of wet plant mass on (a) snails and (b) plants in
experiment 2. Means +1SE. Means with the same letters were not
significantly different in post-hoc tests. L. s. = L. spongia, H. u. = H.
umbellata, A. p. = A. philoxeroides, E. c. = E. crassipes ............................... 61
xi
Figure 4-1 The dependence of plant mass in communities with (a) exotic
plants only or (b) native plants only ,and (c) exotic plant mass and (d)
native plant mass in communities with both native and exotic plants. ....... 85
Figure 4-2 The dependence of percent cover for each native and exotic
plant species on temperature and nutrients in communities with both
native and exotic plants ................................................................................... 86
Figure 4-3 The dependence of (a-b) native and (c-d) exotic plant mass and
diversity on nutrients and community composition. Means +1SE. Means
with the same letters were not significantly different in post-hoc tests.
Np = native plant, ep = exotic plant, np + ep = native and exotic plants in
community ........................................................................................................ 87
Figure 5-1 Exotic P. maculata snail egg clutch mass dependence on (a)
nutrients, (b) temperature, and (c) plant addition treatments over time.
Means ±1SE..................................................................................................... 109
Figure 5-2 Exotic P. maculata snail mass dependence on nutrient and
temperature treatments. Means +1SE. Means with the same letters were not
significantly different in post-hoc tests ........................................................ 110
Figure 5-3 Native P. acuta snail abundance dependence on nutrient
treatments. Means +1SE. Means with the same letters were not significantly
different in post-hoc tests.............................................................................. 111
Figure 5-4 (a) Total plant mass dependence on nutrients together with plant
addition and (b) on temperature together with plant addition treatments. (c)
Native plant mass dependence on nutrients together with plant addition
and (d) on temperature together with plant addition treatments. (e) Exotic
plant mass dependence on nutrients and (f) on temperature. Means +1SE.
Means with the same letters were not significantly different in post-hoc
tests ................................................................................................................. 112
xii
List of Tables
Table 2-1 Description of experimental treatments. Each tank received
topsoil, native plants and native snails in June 2010 and additional plants
and snails in April 2011 and June 2011. Exotic plant or snail additions in
each treatment are shown in bold................................................................... 37
Table 3-1 The dependence of exotic P. maculata snail shell length and
percent mortality in experiment 1 and P. maculata operculum length and
wet plant mass in experiment 2 on nutrients, plants, snails, and their
interactions in ANOVAs. Significant results are shown in bold ................... 58
Table 4-1 The dependence of community composition using plant mass in
native plant only, exotic plant only, and communities with both native and
exotic plants on nutrients, temperature, and their interaction in
PERMANOVAs. Significant results are shown in bold .................................. 81
Table 4-2 The dependence of native and exotic plant mass and diversity
(Shannon Diversity Index) on plant composition, nutrients, temperature,
and their interactions in ANOVAs. Significant results are shown in bold ... 82
Table 4-3 The dependence of exotic to native plant mass ratio on nutrients,
temperature and their interaction, in contrasts of expected ratio from native
only and exotic only plant communities and the observed ratio from
communities with both native and exotic plants. Significant results are
shown in bold ................................................................................................... 83
Table 4-4 The dependence of species cover on nutrients, temperature, and
their interactions in repeated measures ANOVAs using proportional cover
for each species in communities with both native and exotic plants.
Significant results are shown in bold ............................................................. 84
Table 5-1 The dependence of exotic snail P. maculata egg clutch number,
egg clutch mass, adult mass, and native snail P. acuta abundance on
nutrients, temperature, plant addition, and their interactions in ANOVAs or
repeated measures ANOVAs. Significant results are shown in bold ......... 107
Table 5-2 The dependence of total, native, and exotic plant masses on
nutrients, temperature, plant addition, and their interactions in ANOVAs.
Significant results are shown in bold ........................................................... 108
xiii
List of Appendix Figures
Appendix Figure 3-1 The dependence of P. maculata shell length on (a)
nutrients and (b) plants in experiment 1. Means +1SE. Means with the same
letters were not significantly different in post-hoc tests. E. c. = E. crassipes,
A. p. = A. philoxeroides……………………………………….…………………...126
Appendix Figure 3-2 The dependence of (a) L. spongia, (b) H. umbellata, (c)
E. crassipes, and (d) A. philoxeroides wet plant mass on snails in
experiment 2. Means +1SE. Means with the same letters were not
significantly different in post-hoc tests…………………………………...……127
Appendix Figure 4-1 The dependence of exotic (a-b) E. crassipes, (c-d)
A. philoxeroides, and (e-f) P. stratiotes and native (g-h) P. cordata, (i-j)
L. spongia, (k-l) H. umbellata, and (m-n) T. latifolia in relation to nutrient
and temperature in exotic or native only communities and communities
with both native and exotic plants. Symbol size represent species dry plant
mass…………………………………………………………………………………..128
Appendix Figure 4-2 (a) Native L. spongia and (b) exotic E. crassipes mass
dependence on community composition and nutrients. Bars represent
+1SE. Means with the same letters were not significantly different in posthoc tests. Scale is different for each species…………………………………129
Appendix Figure 5-1 Exotic P. maculata snail (a) egg clutch number and (b)
egg mass dependence on the interactive effect of temperature, nutrients,
and plant addition treatments over time. Means ± 1SE……………...………130
Appendix Figure 5-2 Pomacea maculata mass dependence on plant
addition, nutrients, and temperature treatments. Means +1SE…………….131
Appendix Figure 5-3 (a) P. acuta and (b) P. trivolvis dependence on plant
addition, nutrients, and temperature treatments. Means+1SE…………….132
Appendix Figure 5-4 Native (a) H. umbellata (no significant interactive
result), (b) L. spongia, (c) P. cordata, and (d) T. latifolia mass dependence
on nutrients and plant addition treatments. Means +1SE. Means with the
same letters were not significantly different in post-hoc tests. Note that the
y-axis scales differ among species………………………………………….…..133
Appendix Figure 5-5 Exotic (a) E. crassipes, (b) A. philoxeroides, and (c)
P. stratiotes mass dependence on nutrient treatments. Means +1SE. Means
with the same letters were not significantly different in post-hoc tests. Note
that the y-axis scales differ among species…………………….……………..134
xiv
List of Appendix Tables
Appendix Table 3-1 The dependence of native L. spongia and H. umbellata
and exotic A. philoxeroides and E. crassipes wet plant mass in experiment
2 on nutrients, snails, and their interactions in ANOVAs. Significant results
are shown in bold………………………………………………………..…………135
Appendix Table 4-1 The dependence of percent cover on community
composition, nutrients, temperature, and their interaction in repeated
measures ANOVAs. Significant results are shown in bold…………………136
Appendix Table 4-2 The dependence of exotic plant masses on nutrients,
temperature, and their interaction in ANOVAs. Significant results are
shown in bold…………………………………………………..……………………137
Appendix Table 5-1 Total and native plant mass and individual native
species mass dependence on plant addition, nutrient, and temperature.
Exotic plant mass and individual exotic species mass dependence on
nutrients and temperature. Means±SE……………………………………….....138
Appendix Table 5-2 The dependence of native plant masses on nutrients,
temperature, plant addition, and their interactions in ANOVAs. Significant
results are shown in bold…………………………………………………………139
Appendix Table 5-3 The dependence of exotic plant masses on nutrients,
temperature, and their interaction in ANOVAs. Significant results are
shown in bold……………………………………………..…………………………140
15
Chapter 1
Introduction
Ecosystems are often invaded by multiple exotic species. This may reflect exotic
species’ common paths of introduction (Padilla & Williams, 2004; Westphal et al.,
2008), common responses to anthropogenic factors (Mainka and Howard 2010;
Montoya and Raffaelli 2010) or facilitative interactions among exotic species
(Simberloff and Von Holle 1999; Simberloff 2006). Because many ecosystems
are often already invaded by exotic species, it is critical to understand how
established exotic species can affect future exotic species invasions and the
overall impact of multiple exotic species in native ecosystems. In addition,
ecosystems that are invaded by numerous exotic species are simultaneously
threatened by multiple anthropogenic factors. Studies have shown that
anthropogenic factors such as nutrient enrichment and climate warming in
isolation from one another can increase the probability of species invasions.
Studies investigating single anthropogenic factors effects on exotic species
16
increase our knowledge of invasion ecology, but limit our ability to predict the
interactive effect of anthropogenic factors on species invasions and their impacts
on native species. However, studies investigating the effect of multiple
anthropogenic factors is increasing, emphasizing that it is critical to
simultaneously investigate multiple anthropogenic factor effects on species
invasions and their effect on native species because these effects may be
complex. Anthropogenic factors may interact with each other increasing,
reducing, or have no effect on other anthropogenic factors. Therefore, it is critical
to investigate 1) how established exotic species may influence the performance
and invasion success of other exotic species, 2) interactive effects of multiple
anthropogenic factors on exotic species performance and their impact on native
species, and 3) the effect of species invasion and multiple anthropogenic factors
(nutrient enrichment and warming) on native freshwater wetland communities.
I conducted two greenhouse and three field mesocosm experiments to
evaluate the role of species interactions (reciprocal invader facilitation) and the
effect of multiple anthropogenic factors on exotic aquatic plants and an exotic
herbivore and on native aquatic plants and native snails at the population and
community level.
The native and exotic plants and consumers that were included in these
studies co-occur in southeast Texas. The exotic plants include were
Alternanthera philoxeroides (alligator weed - Amaranthaceae), Eichhornia
crassipes (water hyacinth - Pontederiaceae), Pistia stratiotes (water lettuce Araceae), and the exotic snail Pomacea maculata (island apple snails -
17
Ampullariidae; synonym P. insularum) (Hayes et al. 2012). These species heavily
invade local wetlands in southeast Texas. These exotic species co-occur with
native wetland plants that include Hydrocotyle umbellata (water pennywort Araliaceae), Limnobium spongia (frog's bit - Hydrocharitaceae), Pontederia
cordata (pickerelweed - Pontederiaceae), Typha latifolia (cattail - Typhaceae),
and also native snails that include Physa acuta (bladder snail - Physidae) and
Planorbella trivolvis (marsh ramshorn snail - Planorbidae). These native and
exotic plants were selected for these studies based on their clonal reproduction,
functional group (i.e. submerged, emergent, or floating) and co-occur with each
other in the introduced range. Exotic Pomacea maculata, island apple snails, are
voracious generalist plant consumers (Rawlings et al. 2007) with high impacts on
native wetland communities (Meza-Lopez and Siemann 2015) compared to
native snails. These exotic plants and herbivore are sympatric in their native
(South America) and introduced range.
To understand the effect of anthropogenic factors on exotic plants and
P. maculata, I first investigated nutrient enrichment direct and indirect effects on
P. maculata performance. I found that nutrients tended to increased P. maculata
size when they were fed exotic E. crassipes or A. philoxeroides, but P. maculata
size was larger with cut lettuce independent of nutrient treatment, suggesting
nutrient enrichment did not directly affect P. maculata performance. In addition,
P. maculata mortality was lower with lettuce and highest with A. philoxeroides,
suggesting that exotic plants are not an ideal food source for P. maculata.
18
To further understand the effects of nutrient enrichment on P. maculata and
exotic plant performance, I investigated nutrient enrichment effects on exotic
plants E. crassipes and A. philoxeroides mass and exotic snail P. maculata
operculum length. Elevated nutrients increased P. maculata operculum length via
native and exotic plants independent of plant identity. In addition, P. maculata
reduced exotic plant mass, but native plant mass was lower independent of
P. maculata invasions, suggesting that exotic plants would benefit from
P. maculata invasions. Even though we found that P. maculata may benefit
A. philoxeroides invasions and that elevated nutrients increased exotic plant and
herbivore performance, it is critical to understand how nutrient enrichment may
alter species invasions and influence the effect of other anthropogenic factors on
multitrophic exotic species and their effects on native communities.
I investigated the interactive effect of nutrient enrichment and warming on
plant invasions and their effect on native wetland plant communities. Nutrient
enrichment increased plant invasions and warming had no effect. The effect of
nutrient enrichment was higher in communities with exotic plants than in
communities with both native and exotic plants. In addition, the magnitude of
nutrient enrichment effects on exotic species dependent on warming.
Furthermore, nutrient enrichment increased exotic plant mass but only a few
species benefitted from an increase in nutrients. In contrast, warming had no
effect on diversity, suggesting that warming would not influence plant invasions.
Additional studies are necessary to increase our understanding of climate
warming effects on plant invasions with longer field studies. In addition, native
19
and exotic plant mass and diversity was higher in native or exotic plant
communities than in communities with both native and exotic plants with elevated
nutrients. Furthermore, the exotic to native plant mass ratio in communities with
both native and exotic plants was lower than expected from native or exotic plant
communities. Together these results emphasize that it is critical to include native
plant communities to better predict the effect of multiple anthropogenic factors on
plant invasions. Our results suggest that warming will not influence plant
invasions but will influence the effect of nutrient enrichment on exotic species.
Finally, I investigated the interactive effect of anthropogenic factors on
multitrophic exotic species and how these anthropogenic factors influenced
exotic species effects on native plants and snails in wetland communities.
Warming increased P. maculata reproduction four-fold, but had no effect on
exotic plants, suggesting that warming effects can vary depending on exotic
species identity or trophic level. Elevated nutrients increased P. maculata
operculum length and warming increased P. maculata reproduction, suggesting
that the interactive effect of nutrient enrichment and warming cannot be predicted
based on their individual effects. In addition, elevated nutrients increased plant
performance, but had greater effects on exotic plants and also increased native
snail abundance. Native and exotic plant interactions reduced the effect of
elevated nutrients on each other. These results suggest that nutrient enrichment
effects can vary with trophic level and species identity. Therefore, it is critical to
understand the effect of multiple anthropogenic factors on native and exotic
20
plants and native and exotic consumers and how they influence exotic species
effects on native species.
These studies increased our understanding of role of species interactions, the
effect of multiple anthropogenic factors on plant invasions and an exotic
herbivorous snail, and their impacts on native aquatic plants and snails at the
population and community level. These results showed that warming together
with elevated nutrients may increase the probability of aquatic herbivore
invasions, that native plants influence the effect of elevated nutrients on plant
invasions, and that the effect of nutrient enrichment and warming can vary with
species trophic level and species identity. Together these results showed that
nutrient enrichment and warming influence the performance of exotic plants and
exotic herbivores in freshwater wetland communities and that their interactive
effect on plant invasions cannot be predicted based on their individual effects
without considering native communities.
Chapter 2
Experimental test of the Invasional
Meltdown Hypothesis: an exotic
herbivore facilitates an exotic plant, but
the plant does not reciprocally facilitate
the herbivore
Meza-Lopez, M. M. and Siemann, E. (2015), Experimental test of the
Invasional Meltdown Hypothesis: an exotic herbivore facilitates an exotic plant,
but the plant does not reciprocally facilitate the herbivore. Freshwater Biology,
60: 1475–1482. doi: 10.1111/fwb.12582
2.1. Abstract
Ecosystems with multiple exotic species may be affected by facilitative invader
interactions, which could lead to additional invasions (Invasional Meltdown
Hypothesis). Experiments show that one-way facilitation favours exotic species
and observational studies suggest that reciprocal facilitation among exotic
species may lead to an invasional meltdown. We conducted a mesocosm
21
22
experiment to determine whether reciprocal facilitation occurs in wetland
communities. We established communities with native wetland plants and
aquatic snails. Communities were assigned to treatments: control (only natives),
exotic snail (Pomacea maculata) invasion, exotic plant (Alternanthera
philoxeroides) invasion, sequential invasion (snails then plants or plants then
snails) or simultaneous invasion (snails and plants). Pomacea maculata
preferentially consumed native plants so A. philoxeroides comprised a larger
percentage of plant mass and native plant mass was lowest in sequential (snail
then plant) invasion treatments. Even though P. maculata may indirectly facilitate
A. philoxeroides, A. philoxeroides did not reciprocally facilitate P. maculata.
Rather, ecosystems invaded by multiple exotic species may be affected by oneway facilitation or reflect exotic species’ common responses to abiotic factors or
common paths of introduction.
2.2. Keywords
invasional meltdown, reciprocal facilitation, Pomacea maculata, Alternanthera
philoxeroides, experimental wetlands
2.3. Introduction
Ecosystems are often invaded by multiple exotic species. This may reflect exotic
species’ common paths of introduction (Padilla and Williams 2004; Westphal et
al. 2008), common responses to abiotic factors (Mainka and Howard 2010;
Montoya and Raffaelli 2010) or facilitation among exotic species (Simberloff and
23
Von Holle 1999; Simberloff 2006). Because many ecosystems are often already
invaded by exotic species, it is critical to know how established exotics affect
future invasions and to understand the overall impact of multiple exotic species in
an ecosystem. An established exotic species may increase the susceptibility of
ecosystems to future invasions by altering biotic and/or abiotic characteristics of
an invaded habitat (Simberloff and Von Holle 1999; Grosholz 2005). If such
facilitation of subsequent exotic species is common, this may lead to an
invasional meltdown where exotic species facilitate other exotic species by
increasing their likelihood of survival and/or their ecological impacts, including the
magnitude of their impacts, as proposed by the Invasional Meltdown Hypothesis
(IMH hereafter) (Simberloff and Von Holle 1999). Simberloff (2006) suggested
that various degrees of facilitation, ranging from simple facilitation (one exotic
species aiding the invasion of another) to reciprocal facilitation (exotic species
increasing each other’s performance), could lead to an invasional meltdown.
Reciprocal facilitation is a type of facilitation and an aspect of the IMH that
remains controversial because experimental studies have yet to show evidence
of reciprocal facilitation among exotic species that leads to an invasional
meltdown (Simberloff 2006; Gurevitch 2006).
Studies supporting the IMH show evidence of one-way facilitation between
exotic species (Ricciardi et al. 2013) that may occur via consumptive or nonconsumptive mechanisms. For instance, exotic red deer (Cervus elaphus) and
fallow deer (Dama dama) indirectly facilitated exotic Douglas fir (Pseudotsuga
menziesii) by preferentially consuming the native evergreen conifer Austrocedrus
24
chilensis (Relva et al. 2009). In addition, crayfish (Orconectes rusticus) may
facilitate the invasion of exotic Eurasian watermilfoil (Myriophyllum spicatum) by
increasing plant fragmentation (non-consumptive) (Maezo et al. 2010). Likewise,
exotic plants may facilitate exotic herbivores by providing a higher quality food
source (Engelkes and Mills 2013) or by supplying higher quality substrata for
reproduction (Burks et al. 2010) or shelter (Sessions and Kelly 2002). These
studies showed that exotic species can facilitate other invaders; however, they
did not investigate whether reciprocal facilitation occurred.
An invasion meltdown may occur via reciprocal facilitation among exotic
species as suggested by field surveys (O’Dowd et al. 2003; Green et al. 2011) or
via one-way facilitation among exotic species, increasing the frequency of
additional invasions (Simberloff, 2006; Helms, Hayden & Vinson, 2011). A recent
study evidenced a newly formed mutualism between two exotic species where
the yellow crazy ant Anoplolepis gracilipes protects exotic scale insects and
scales produce honeydew that ants consume (O’Dowd et al. 2003). Exclusion of
A. gracilipes reduced the abundance of exotic scale insects (Abbott and Green
2007), but the effects of the scale insect on A. gracilipes are yet to be
investigated. In addition, an exotic grass (Cynodon dactylon) increased the
abundance of exotic honeydew-producing mealybug (Antonina graminis) that in
turn may increase the abundance of exotic fire ants (Solenopsis invicta) that tend
A. graminis; however, A. graminis did not affect the performance of C. dactylon
(Helms et al. 2011). These studies suggest that exotic species may facilitate
25
other exotic species, contributing to an invasional meltdown, without their effects
being reciprocal.
The effects of established exotic species on subsequent invasions may
influence their impact on native species (Johnson et al. 2009; Green et al. 2011).
For instance, the exotic rusty crayfish Orconectes rusticus and exotic Chinese
mystery snail Bellamya chinensis had weak negative effects on each other, but
together they drove a native snail to extinction and reduced the abundance of
another snail by 95% (Johnson et al. 2009). These interactive effects were due to
facilitative interactions between invaders. Similarly, exotic scale insects
(Tachardina aurantiaca and Coccus spp.) may facilitate A. gracilipes invasions,
reducing native red land crab (Gecarcoides natalis) abundance and increasing
the probability of exotic giant African land snail Achantina fulica invasions
(O’Dowd et al. 2003; Green et al. 2011). These studies suggest that the
co-occurrence of multiple exotic species could have greater consequences on
native species than their individual impacts (Johnson et al. 2009).
Here, we investigated whether reciprocal facilitation between exotic species
contributes to an invasional meltdown in wetland mesocosm communities.
Specifically, we evaluated whether an exotic plant (Alternanthera philoxeroides)
and an exotic generalist herbivorous snail (Pomacea maculata) reciprocally
facilitate each other and whether their impact on native plants is non-additive.
26
2.4. Methods
2.4.1. Study system
In south east Texas, Alternanthera philoxeroides (alligator weed Amaranthaceae) and Pomacea maculata (island apple snails – Ampullariidae;
synonym P. insularum) heavily invade local wetlands, co-occurring with native
wetland plants Hydrocotyle umbellata (water pennywort – Araliaceae),
Limnobium spongia (frog's bit – Hydrocharitaceae), Myriophyllum pinnatum
(cutleaf watermilfoil - Haloragaceae) and Pontederia cordata (pickerelweed –
Pontederiaceae) with native snails Haitia acuta (Physidae – synonyms include
Physa acuta and Physella acuta).
Alternanthera philoxeroides was introduced to the USA in ballast water from
the Parana River region of South America (Julien et al. 1995). It was first
recorded in Mobile, Alabama in 1897; by 1963, it had invaded coastal states from
North Carolina to Texas (Spencer and Coulson 1976). In aquatic habitats, it
anchors to banks and reproduces clonally, but does not produce viable seeds in
its introduced range (Spencer and Coulson 1976; He et al. 2014). Alternanthera
philoxeroides can form extensive interwoven mats from plant fragments that can
become independent free-floating monocultures (Spencer and Coulson 1976;
Sainty et al. 1997).
Thought to be introduced via the aquarium trade, Pomacea maculata was
discovered in 1989 in south east Texas with source populations probably from
the lower Parana River Basin in La Plata region of Argentina (Hayes et al. 2012).
27
Its native range extends north to the Amazon basin of Brazil, north of Manaus,
and also occurs in Uruguay and Paraguay (Hayes et al. 2008; Karatayev et al.
2009; Hayes et al. 2012). Pomacea maculata populations have been reported
along the Gulf Coast from Texas to Florida and along the Atlantic coast to South
Carolina (Rawlings et al. 2007; Byers et al. 2013). Unlike native aquatic snails
that primarily consume periphyton, P. maculata is a generalist voracious plant
consumer (Rawlings et al. 2007). Pomacea maculata’s impact on native
ecosystems is currently unknown.
2.4.2. Establishing native wetland communities
In June 2010, we established forty wetland communities in 473 L tanks (Poly
tank, round flat-bottom nestable tanks, Litchfield, MN, USA) in an open
greenhouse structure at the Rice University South Campus Field Station (29.6 N,
95.4 W). To prepare the greenhouse structure, three layers of poly cloth floor
were attached to boards that were secured on the bottom perimeter of the
greenhouse frame. To each tank, we added 15 cm of topsoil, municipal water,
115 native snails and native plants (H. umbellata, L. spongia, M. pinnatum and
P. cordata – one individual of each). Water was allowed to sit for a week before
plants and snails were added. Dechlorinator was added to subsequent water
additions, which were necessary to maintain water levels constant for the
duration of the study. Plants that did not survive the initial planting were replaced
to ensure that all species were included in the communities. Native plants and
snails were allowed to establish for 10 months. Native Utricularia inflata
(bladderwort) invaded some tanks, perhaps from the waterfowl that occasionally
28
landed in tanks; therefore, it was added to all uninvaded tanks to reduce variation
among communities. After plants were established, the open greenhouse
structure was enclosed with fiberglass screen (Metro Screenworks, Englewood,
CO, USA) attached to secured boards to tightly seal the entire greenhouse
structure. The fiberglass screen reduced incoming radiation by fifty percent.
2.4.3. Exotic species
Pomacea maculata egg clutches and A. philoxeroides plants were collected in
Armand Bayou in Pasadena, Texas, USA (29.6 N, 95.1 W). Females emerge
from water at night to lay egg clutches on solid objects above the water level. To
simulate natural hatching conditions in the laboratory, collected egg clutches
were placed on top of a plastic mesh with small holes above a container partially
filled with water. This allowed P. maculata to fall into water as they hatched. They
were reared on commercial romaine lettuce until they reached the desired size
for the study (Morrison and Hay 2011).
2.4.4. Experimental manipulation
In April 2011, established communities were randomly assigned to the following
treatments: (1) control (only natives) [C], (2) invasion by plants (A. philoxeroides)
[P] or snails (P. maculata) [S], (3) simultaneous invasion of plants and snails
[P & S] or (4) sequential invasion: plants then snails [P - S] or snails then plants
[S - P]. Single invasion treatments were replicated eight times, while other
treatments were replicated six times. Replicates were limited by the number of
tanks available. Every tank received plants collected from the same location in
29
April and June 2011, so that plant invasion treatments only manipulated plant
origin (native or exotic) (Table 2-1). Plant additions were always 60 g of plant
mass independent of plant origin. Snail invasion treatments were either three
P. maculata, simulating natural densities in lotic waters in south east Texas
(Howells et al. 2006), or 20 native snails. Pomacea maculata on average
weighed 27 g with an average operculum length of 25 mm, while native snails
were much smaller (~5 mm).
Weekly P. maculata egg clutch surveys were conducted throughout the study
to measure and quantify egg clutches and record the location of egg clutch
oviposition. Total egg clutch volume per tank was estimated as the sum of the
products of length, width and thickness of each egg clutch. In August 2011, we
removed, sorted by species and oven-dried aboveground plant mass. Native
plant diversity was calculated using the Shannon Diversity Index. Adult
P. maculata were collected, weighed and measured. Native snail and juvenile
P. maculata abundances were estimated by collecting as many snails as
possible in fifteen minutes. Such incomplete sampling of snails could increase
the possibility of a type II error. Collected snails were sorted by size and counted
in the laboratory.
2.4.5. Data analyses
Analysis of variance (ANOVA) was used to test the dependence of exotic plant
variables (exotic plant dry mass and plant mass as a percent of total mass,
excluding native plant mass), exotic snail performance (operculum length, adult
mass, total egg clutch volume and juvenile abundance), native plant variables
30
(plant dry mass and diversity, excluding exotic plant mass) and native snail
abundance on invasion treatments (P<0.05). Data met the assumptions of
ANOVA. Exotic plant ANOVAs included only treatments with plant invasions in
June 2011 ([P], [S - P] and [P & S]). Exotic snail ANOVAs only included
treatments with snail invasions in June 2011 ([S], [P - S] and [P & S]). [P & S]
invasion treatments were included in both exotic plant and exotic snail ANOVAs.
Tukey-Kramer multiple comparison tests were conducted to determine the
differences between treatment levels (P<0.05) for significant variables with more
than two levels.
We performed additional two-way ANOVAs to examine whether the impacts
of A. philoxeroides and P. maculata on native plant mass and diversity and native
snail abundance were non-additive (i.e. non-independent). These interactive
ANOVAs included only [C], [P], [S] and [P & S] invasion treatments and exotic
snail presence, exotic plant presence and their interaction as predictors. A
significant interaction between predictors indicates non-additive impacts (i.e. the
combined effect of the species is different from the sum of each species’
individual impacts). All statistical analyses were performed using StatView
(v 5.0).
2.5. Results
2.5.1. Reciprocal facilitation between exotic species (IMH)
Pomacea maculata in sequential [S - P] and simultaneous [P & S] invasion
treatments reduced A. philoxeroides dry mass (F2,17 = 9.5, P = 0.0017;
31
Figure2-1a), but A. philoxeroides mass as percent total plant mass was highest
in sequential [S – P] invasion treatments (F2,17 = 4.0, P = 0.0373, Figure 2-1b). By
contrast, native plant dry mass was lowest in sequential [S – P] invasion
treatments (F5,34 = 11.8, P < 0.0001; Figure 2-2a).
Alternanthera philoxeroides did not facilitate the invasion of P. maculata.
Alternanthera philoxeroides did not affect P. maculata’s operculum length
(F2,17 = 1.8, P = 0.1931; Figure 2-3a), adult mass (F2,17 = 0.5, P = 0.6349; Figure
2-3b), total egg clutch volume (F2,17 = 0.5; P = 0.6378; Figure 2-3c) or juvenile
abundance (F2,17 = 0.9, P = 0.4095; Figure 2-3d).
2.5.2. Exotic species impacts
Pomacea maculata together with exotic plant invasions had greater effects on
native plants than did A. philoxeroides invasions alone. Native plant diversity was
lowest in simultaneous [P & S] invasion treatments (F5,34 = 14.3, P < 0.0001;
Figure 2-2b). Pomacea maculata significantly reduced native plant mass
(F1,24 = 15.2, P < 0.0007) and diversity (F1,24 = 35.5, P < 0.0001), while
A. philoxeroides did not affect native plant mass (F1,24 = 2.5, P = 0.13) or diversity
(F1,24 = 0.5, P = 0.50). Together these exotic species had additive impacts on
native plant mass (snail*plant: F1,24 < 0.1, P = 0.8379) and diversity
(snail*plant: F1,24 = 0.7, P = 0.4161) as indicated by non-significant interaction
terms. No factors influenced native snail abundance (all P > 0.59).
32
2.6. Discussion
2.6.1. Reciprocal facilitation between exotic species (IMH)
Multiple exotic species in these wetland communities are not a result of
reciprocal facilitation. Alternanthera philoxeroides did not affect the size, survival,
reproduction or population growth of P. maculata. In addition, P. maculata
directly limited the abundance of A. philoxeroides. However, P. maculata’s
preferential consumption of native plants may indirectly facilitate A. philoxeroides
invasions by reducing native plant competition. Other studies show that exotic
herbivores, including exotic slugs (Hahn et al. 2011; Hahn et al. 2011), deer
(Nuñez et al. 2008; Relva et al. 2009), gypsy moths (Lymantria dispar) (McEwan
et al. 2009) and snails (Motheral and Orrock 2010), may facilitate plant invasions
by preferentially consuming native plants. This suggests that exotic herbivore
facilitation of exotic plants is a common pattern that may reflect the traits of exotic
plants, the traits of exotic herbivores or more complex mechanisms
(Pearse et al. 2013).
Exotic herbivores may also directly facilitate exotic plants via
non-consumptive mechanisms. For instance, plant fragmentation may increase
the dispersal of exotic plants (Maezo et al. 2010). A greenhouse study showed
that mechanically generated A. philoxeroides’ single-node fragments survived
and grew in a moist soil mix, so fragmentation may increase the rate of spread of
this clonal species (Dong et al. 2012). Here, P. maculata reduced
A. philoxeroides’ mass, but also generated plant fragments that could increase
33
the spread of A. philoxeroides to new patches in open, natural conditions, or
contribute to existing patches. In the introduced range, the only herbivore other
than P. maculata that commonly feeds on A. philoxeroides is the alligator weed
flea beetle Agasicles hygrophila (Schooler et al. 2006). The beetle preferentially
feeds on the young leaves and stem tissue of A. philoxeroides, but does not
generate nodal fragments (Schooler et al. 2006). Our experiment did not
consider local negative effects or distant positive effects of dispersal from
A. philoxeroides fragmentation by P. maculata. It is possible that P. maculata’s
feeding may facilitate A. philoxeroides’ spread and invasions by creating nodal
fragments that could contribute to existing patches and the establishment of new
patches.
Exotic plants did not directly facilitate exotic herbivore invasions in native
plant dominated wetlands. Pomacea maculata’s survival, growth (operculum
length and adult mass), reproduction (total egg clutch volume) and juvenile
abundance were all independent of A. philoxeroides invasions. These results are
not a strong test of the direct effects of A. philoxeroides on P. maculata when the
exotic plant is abundant because P. maculata preferentially consumed native
plants more than A. philoxeroides. Even though A. philoxeroides did not directly
facilitate P. maculata invasions, other exotic plants that co-occur with
P. maculata in the introduced range may facilitate P. maculata invasions. For
instance, a feeding trial showed that P. maculata could survive and grow when
offered the exotic plants Eichhornia crassipes, C. esculenta or M. spicatum,
although it consumed little E. crassipes and C. esculenta (Burks et al. 2011). In
34
contrast, a feeding trial in China showed that P. canaliculata, another apple snail,
had low survival and did not grow or reproduce when reared on E. crassipes,
M. aquaticum or C. esculenta (Qiu and Kwong 2009). Studies on the facilitative
effects of exotic plants on exotic herbivores through consumptive mechanisms
are inconclusive. However, exotic plants may facilitate exotic herbivorous snails
through non-consumptive mechanisms. For example, C. esculenta may indirectly
facilitate P. maculata by providing substrata for egg oviposition (Burks et al.
2010). In our study, A. philoxeroides did not seem to be a preferred oviposition
substratum because all P. maculata egg clutches were oviposited on the sides of
tanks or on native P. cordata leaves and stems. Although the invasion of
P. maculata was independent of A. philoxeroides, the wide variety of plant
architecture and plant chemistry represented in exotic aquatic plants that
co-occur with P. maculata leaves open the possibility that other exotic plants may
facilitate or inhibit P. maculata invasions (Pearse et al. 2013).
2.6.2. Exotic species impacts
Exotic herbivores affected native plants in all treatments by decreasing native
plant mass and diversity independent of A. philoxeroides invasions. Similarly, a
feeding trial showed that P. maculata consumed native plants (Ceratophyllum
demersum, Hymenocallis liriosme, Ruppia maritima and Sagittaria lancifolia) and
exotic plants (C. esculenta, A. philoxeroides and E. crassipes), but consumption
of native plants was higher (Burlakova et al. 2009). However, another study
showed that P. maculata did not differentially consume native and exotic plants
(Qiu and Kwong 2009). Pomacea canaliculata has had severe impacts on native
35
plants (Lowe et al. 2004), transforming native wetlands in Thailand into open
water habitats without plants (Carlsson et al. 2004). Our recorded effects of
P. maculata on wetlands are comparable to those of P. canaliculata because
P. maculata significantly reduced native plant mass and diversity in wetland
communities.
In contrast, A. philoxeroides only affected native plants in the presence of
P. maculata. Other studies have shown that A. philoxeroides reduces native plant
diversity in weedy habitats (Lin and Qiang 2006), native plant cover in aquatic
habitats in New Zealand (Bassett et al. 2012) and species richness, diversity and
evenness in India (Chatterjee and Dewanji 2014). The duration of a study and
the initial exotic plant mass may influence the outcome of native and exotic plant
interactions. Indeed, a longer experiment might provide a more conclusive test.
Even though A. philoxeroides’ effects on native plants were greater with prior
P. maculata invasions, their combined effect in the simultaneous [S & P] invasion
treatment was additive. Johnson et al. (2009) also found that the effect of
multiple exotic species on native species is greater than the effect of a single
exotic species and greater effects of invaders from higher trophic levels. This
suggests that exotic consumers with large consumptive effects on native species
can facilitate lower trophic invaders, leading to multiply invaded ecosystems.
2.7. Acknowledgments
We thank Steve Pennings for tanks; Candice Tiu, Nick Hill, Dana Galvan, Ariel
Nixon, Erica Soltero and Leiyi Chen for assistance in the field and lab; Xin-Min Lu
36
for helpful comments; Romi Burks, Jenn Rudgers, Amy Dunham, Volker Rudolf
and Anna Armitage for helpful discussions and two anonymous reviewers for
comments. This work was supported by a Ford Foundation Predoctoral
Fellowship (to MML), an Environmental Protection Agency Science to Achieve
Results Fellowship for Graduate Environmental Study (to MML), a Constance E.
Boone Graduate Student Research grant from the Houston Conchology Society
(to MML), a Society of Wetland Scientist Graduate Research grant (to MML) and
a Kroger Community Donation (to MML).
Table 2-1 Description of experimental treatments. Each tank received topsoil, native plants and native snails in
June 2010 and additional plants and snails in April 2011 and June 2011. Exotic plant or snail additions in each
treatment are shown in bold
Treatment
April 2011
June 2011
Control [C]
60 g native plants
20 native snails
60 g native plants
20 native snails
Plant invasion [P]
60 g native plants
20 native snails
60 g exotic plants
20 native snails
Snail invasion [S]
60 g native plants
20 native snails
60 g native plants
3 exotic snails
Simultaneous invasion-plants
and snails [P&S]
60 g native plants
20 native snails
60 g exotic plants
3 exotic snails
Sequential invasion-plants
then snails [P–S]
60 g exotic plants
20 native snail
60 g native plants
3 exotic snails
Sequential invasion-snails
then plants [S–P]
60 g native plants
3 exotic snails
60 g exotic plants
20 native snails
37
30
(a)
single
a
sequential
simultaneous
b
b
20
10
0
P
S-P
Invasion treatment
P&S
A. philoxeroides mass (% of total)
A. philoxeroides dry mass (g)
40
10
(b)
sequential
b
8
6
single
a
simultaneous
a
4
2
0
P
S-P
P&S
Invasion treatment
Figure 2-1 (a) Alternanthera philoxeroides dry mass and (b) mass as
percent of total plant mass in treatments with exotic plants introduced in
June 2011. Means + 1 SE. Means with the same letter were not significantly
different in post-hoc tests. P = exotic plant, S – P = exotic snail invasion
followed by exotic plant invasion, P & S = simultaneous exotic plant and
exotic snail invasion
38
(a)
Native plant dry mass (g)
800
a
single
sequential
ab
bc
600
simultaneous
c
c
d
400
200
0
C
(b)
P
S
P-S S-P
P&S
Native plant diversity
1.5
a
1.2
a
b
b
b
0.9
c
0.6
0.3
0.0
C
Native snail abundance
(c)
P
S
P-S S-P
P&S
P
S
P-S S-P
P&S
800
600
400
200
0
C
Invasion treatment
Figure 2-2 (a) Native plant dry mass and (b) diversity in each invasion
treatment. Means + 1 SE. Means with the same letter were not significantly
different in post-hoc tests. C = native plants and native snails, P = exotic
plant, S = exotic snail, P – S = exotic plant invasion followed by exotic snail
invasion, S – P = exotic snail invasion followed by exotic plant invasion,
P & S = simultaneous invasion by exotic plant and exotic snail
39
150
(a)
single
40
sequential
30
20
(b)
single
simultaneous
Adult mass (g)
Adult operculum length (mm)
50
simultaneous
100
50
10
0
0
S
P-S
P&S
S
Invasion treatment
200
(c)
(d)
sequential
single
150
100
P&S
simultaneous
simultaneous
250
200
P-S
Invasion treatment
Juvenile abundance
300
Egg clutch volume (ml)
sequential
150
single
100
sequential
50
50
0
0
S
P-S
P&S
Invasion treatment
S
P-S
P&S
Invasion treatment
Figure 2-3 (a) Pomacea maculata operculum length, (b) adult mass, (c)
reproductive output (total egg volume) and (d) juvenile abundance were
independent of A. philoxeroides invasions when snails were introduced in
June 2011. Means + 1 SE. S = exotic snail, P – S = exotic plant invasion
followed by exotic snail invasion, P & S = simultaneous invasion by exotic
plant and exotic snail
40
Chapter 3
Nutrient enrichment increased exotic
snail Pomacea maculata growth
independent of native and exotic wetland
plant identity
3.1. Abstract
Ecosystems invaded by many exotic species are often simultaneously exposed
to other anthropogenic factors. Invaders may have common positive responses
to anthropogenic factors that directly and indirectly increase exotic herbivore and
exotic plant performance and also alter plant-herbivore interactions. We
conducted two freshwater mesocosm experiments. In experiment one, we
investigated nutrient enrichment effects on exotic herbivorous snails (Pomacea
41
42
maculata) fed detached lettuce leaves or grown with a single exotic plant species
(Eichhornia crassipes or Alternanthera philoxeroides). Snail shell length varied
with nutrients (control, low, or high), plant type, and their interactions. Nutrients
did not affect shell length of snails fed lettuce, suggesting no direct nutrient
enrichment effects on snail growth. However, snail mortality varied with plant
species, suggesting that snail performance also depends on plant identity. In
experiment two, we investigated: 1) nutrient enrichment effects on snail
operculum length fed a single native (Limnobium spongia or Hydrocotyle
umbellata) or exotic (E. crassipes or A. philoxeroides) plant species and 2) the
effect of nutrient enrichment and exotic snail interactions on native and exotic
plants. Elevated nutrients increased snail operculum length, but nutrients did not
affect plant mass. Snails reduced plant mass, but plant mass was higher for
exotic plants than native plants independent of snail and nutrient treatments,
suggesting that these exotic plants may survive and grow in habitats with varying
environmental conditions. Together these results suggest that nutrient
enrichment will increase exotic herbivore growth and may contribute to multiple
plant invasions, resulting in multiply invaded freshwater wetland ecosystems.
3.2. Keywords
nutrient enrichment • Pomacea maculata • Alternanthera philoxeroides •
Eichhornia crassipes • indirect effects • plant-herbivore interactions
43
3.3. Introduction
Ecosystems invaded by many exotic species are often simultaneously exposed
to other anthropogenic factors. Multiple invasions may be a result of exotic
species’ common responses to anthropogenic factors (Mainka and Howard 2010;
Montoya and Raffaelli 2010). For instance, plant invasions are often associated
with nutrient enrichment (Tyler et al. 2007) because elevated nutrients favor
exotic plants that possess traits that include rapid growth rate, low tissue
production cost, and high phenotypic plasticity compared to resident native plants
(Daehler 2003). However, our knowledge of nutrient enrichment’s direct and
indirect effects on higher trophic levels, including exotic herbivores, is limited
(Alonso and Camargo 2003). To better predict and understand exotic herbivore
invasions, we need to increase our understanding of how anthropogenic factors
such as nutrient enrichment directly and indirectly via plants affect exotic
herbivore survival and growth.
Nutrient enrichment’s direct effects on exotic herbivores are rarely
investigated (Ebeling et al. 2013), but indirect effects via plants have been
examined for native herbivores and on herbivores used as biocontrol agents.
Nutrient enrichment may directly and indirectly affect exotic herbivore survival,
growth, or reproduction, but our understanding of some of these effects is limited.
For instance, an experimental study showed that elevated nutrients increased
native aquatic snail mortality due to higher toxicity levels with elevated nutrient
levels (Alonso and Camargo 2003). Similarly, studies on the indirect effects of
nutrient enrichment on exotic herbivores via exotic plants are limited. Studies
44
evaluating nutrient enrichment indirect effects on herbivores often focus on
herbivores that have been introduced to control and manage troublesome exotic
plants, biocontrol agents. For example, nutrient enrichment increased foliar
nitrogen in exotic plant water hyacinth (Eichhornia crassipes) which resulted in a
shift of water hyacinth grasshopper (Cornops aquaticum), E. crassipes’ biocontrol
agent, sex ratio towards females and increased female fecundity and body mass
(Bownes et al. 2013a). Similarly, nutrient enrichment effects on E. crassipes
increased the population growth and reproduction of weevils Neochetina
eichhorniae and N. bruchi, biocontrols of E. crassipes (Center and Dray 2010).
Together these studies emphasize that our understanding of the direct and
indirect effects of nutrient enrichment on exotic herbivores is limited.
Exotic herbivores may influence exotic plant invasions via several
mechanisms, including higher consumptive effects on co-occurring native plants
(Nuñez et al. 2010) and via non-consumptive effects on exotic plants. For
instance, exotic red deer (Cervus elaphus) and fallow deer (Dama dama)
enhanced the invasion of exotic Douglas fir (Pseudotsuga menziesii) by
preferentially consuming native evergreen conifer (Austrocedrus chilensis) (Relva
et al. 2009). In addition, non-consumptive damage by exotic crayfish
(Orconectes rusticus) on exotic Eurasian watermilfoil (Myriophyllum spicatum)
increased the probability of plant dispersal via plant fragmentation allowing plants
to colonize and invade surrounding habitats (Maezo et al. 2010). Exotic plants
may also influence exotic herbivore performance. For example, exotic plants
increased larval survival and pupal weight and reduced development time of the
45
exotic generalist herbivore Epiphyas postvittana when compared to native plants
(Engelkes and Mills 2013). Together these studies show that exotic herbivores
may influence plant invasions via different mechanisms and that exotic plants
may influence the performance of exotic herbivores.
Studies have shown that the effect of biocontrol agents, special cases of
introduced herbivores, on exotic plants can vary with nutrient availability
(Coetzee et al. 2007; Bownes et al. 2013b). Elevated nutrients increased
E. crassipes growth and reproduction and increased the population growth of
biocontrol mirid (Eccritotarsus catarinensis) (Coetzee et al. 2007). In addition,
elevated nutrients also increased E. catarinensis damage on E. crassipes but the
effect of E. catarinensis on E. crassipes’ performance did not vary with nutrient
levels (Coetzee et al. 2007). Nutrient enrichment and exotic herbivores
interactions may alter their individual effects on exotic plants. For instance, exotic
herbivore effects may be greater at low nutrient levels because exotic plants do
not have the resources needed to recover quickly form herbivore damage. For
example, exotic E. crassipes’ performance was lower at low nutrients with
biocontrol C. aquaticum herbivory (Bownes et al. 2013b). In addition, exotic
herbivore effects on exotic plants may be less severe with high resource
availability because plant may have the resources needed to recover more
quickly from herbivore damage. These studies showed that elevated nutrients
alone increased exotic plant mass, biocontrol herbivores alone reduced exotic
plant mass, but in combination they altered each other’s effects. These studies
guide our predictions on the effects of exotic herbivores on exotic plants, but
46
studies on the effect of exotic herbivore and nutrient enrichment interactions on
exotic plants are needed to predict exotic plant and exotic herbivore
performance, probability of invasion success, and their impacts on native species
in invaded ecosystems.
Here, we conducted two greenhouse mesocosm experiments to investigate:
1) direct and indirect effects of nutrient enrichment on exotic aquatic snail
survival and growth with living and non-living plants and 2a) nutrient enrichment
effects on snail growth with single native or exotic aquatic plant species and 2b)
effects of nutrient enrichment and exotic aquatic snail interactions on native and
exotic plants from freshwater wetland ecosystems.
3.4. Methods
3.4.1. Study system
In southeast Texas, exotic aquatic plants and snails heavily invade local
freshwater wetlands. Exotic species that co-occur in this region include the exotic
plants Alternanthera philoxeroides (alligator weed - Amaranthaceae), Eichhornia
crassipes (water hyacinth - Pontederiaceae), and the exotic snail Pomacea
maculata (island apple snail - Ampullariidae; synonym P. insularum; (Hayes et al.
2012). These exotic plants and snails are sympatric in their native (South
America) and introduced ranges (USA). These exotic species co-occur with
native aquatic plants that include Hydrocotyle umbellata (water pennywort Araliaceae) and Limnobium spongia (frog's bit - Hydrocharitaceae) in southeast
Texas. Native H. umbellata and exotic A. philoxeroides were included because
47
they are both emergent plants that can grow in terrestrial and aquatic habitats
and also co-occur in wetland ecosystems. Native L. spongia and exotic
E. crassipes were included in this study because they are both free-floating
aquatic plants with clonal reproduction and similar plant structure with leaves
above the water surface.
Alternanthera philoxeroides is native to the Parana River region of South
America (Julien et al. 1995) and was first recorded in Mobile, Alabama, USA in
1897 and invaded coastal states from North Carolina to Texas by 1963 (Spencer
and Coulson 1976). In aquatic habitats, A. philoxeroides anchors to banks and
reproduces clonally, but does not produce viable seeds in its introduced ranges
(Spencer and Coulson 1976; He et al. 2014). It has hallow stems that can root at
the nodes when fragmented resulting in large interwoven mats or free-floating
monocultures (Spencer and Coulson 1976; Sainty et al. 1997).
Eichhornia crassipes is considered one of the worst aquatic weeds in the
world with high socio-economic and ecological impacts (Lowe et al. 2004). It was
introduced from South America to the USA in 1884, invaded southern USA states
by the 1900’s, and its current distribution includes more than 50 countries on five
continents (Lowe et al. 2004). This perennial herb is characterized by
free-floating rosettes with clonal reproduction. Newly formed rosettes break
easily, allowing E. crassipes to disperse and colonize neighboring habitats.
Pomacea maculata’s native range expands north to the Amazon basin of
Brazil and occurs in Uruguay, Paraguay, and Argentina (Hayes et al. 2008;
Karatayev et al. 2009). It was discovered in 1989 in southeast Texas with source
48
populations likely from the lower Parana River Basin in La Plata region of
Argentina (Hayes et al. 2012). Pomacea maculata populations have been
reported along the Gulf Coast from Texas to Florida and along the Atlantic coast
to South Carolina (Rawlings et al. 2007; Byers et al. 2013). It has been shown to
have negative effects on several native freshwater wetland plants (Meza-Lopez
and Siemann 2015).
3.4.2. Experimental set-up
We conducted two mesocosm experiments in a temperature-controlled
greenhouse at Rice University, Texas. We collected exotic plants and
P. maculata egg clutches from Armand Bayou (Pasadena, TX). To simulate
natural P. maculata hatching conditions in lab, we placed egg clutches on a
mesh on top of a container that was partially filled with water; snails fell into the
water as they hatched. They were reared on commercially purchased romaine
lettuce until enough juvenile snails were available for each experiment (Conner et
al. 2008). Native plants in the second experiment were commercially purchased.
3.4.3. Exp.1: Nutrients’ direct and indirect effects on P. maculata mortality
and shell length
Experiment 1 was conducted in fall 2009 with forty-five 19L containers filled with
~11.4L of dechlorinated municipal water. Fifteen juvenile P. maculata (~6-7mm
initial foot length) were added to each mesocosm. Mesocosms were randomly
assigned to: 1) nutrients: control (ambient nutrients in municipal water), low
(0.5mg/L Nitrogen and 1mg/L of Phosphorus), or high (5mg/L Nitrogen and
49
10mg/L Phosphorus) and 2) plants: detached non-living lettuce leaves without
roots or a single living exotic plant with roots (A. philoxeroides or E. crassipes)
with five replicates per treatment in a factorial design. Nitrogen treatments were
selected based on nutrient levels in aquatic ecosystems in southeast Texas.
Phosphorus levels selected were higher than levels in Texas during non-drought
conditions, but are typical of phosphorus levels during drought conditions.
Including higher phosphorus levels would increase our understanding of the
effects of nutrient enrichment under varying environmental conditions. Exotic
plant treatments received 25g of a living exotic plant a single time and lettuce
treatments received cut lettuce biweekly to refresh and replenish lettuce
consumed by snails. Cut lettuce was used to investigate direct effects of nutrient
enrichment on P. maculata because cut lettuce without roots is unlikely to absorb
significant amounts of water nutrients before snails consume it compared to
exotic living plants that have roots. Pomacea maculata hatchlings may feed on
periphyton but switch to plants with increasing size. We replaced ~7.57L of water
and replenished nutrients weekly to reduce snail waste accumulation and to
maintain nutrient levels constant throughout the study. After nine weeks, we
counted and measured snail shell length from apex to aperture end (Conner et
al. 2008) and weighed exotic plants.
3.4.4. Exp. 2: Nutrient enrichment effects on P. maculata, plants, and
plant-herbivore interactions
Experiment 2 was conducted at the end of summer 2010 with ninety-six 19L
containers filled with ~11.4L of dechlorinated municipal water. Mesocosms were
50
randomly assigned to: 1) plant treatment: a single native (L. spongia or
H. umbellata) or exotic (E. crassipes or A. philoxeroides) plant; 2) nutrient
treatment: control (ambient nutrients in municipal water), low (3mg/L N and
1mg/L of P), or high (6mg/L N and 2mg/L P); and 3) snail treatment: absence or
presence (10 juvenile P. maculata) in a factorial design with four replicates per
treatment. Mesocosms received the following plant mass depending on plant
treatments: L. spongia = 20.60±0.06g, H. umbellata = 20.35±0.06g, E. crassipes
= 20.47±0.07g, or A. philoxeroides = 20.50±0.05g a single time. Nutrient levels
selected differed from experiment 1 to further assess the effects of nitrogen and
phosphorus levels that are typical in southeast Texas on exotic species
performance. Water was changed weekly as described in experiment 1. After six
weeks, we measured snail operculum length and weighed native and exotic plant
mass. Snail operculum length was used instead of shell length to quantify snail
growth in experiment 2 because snail operculum length was recommended as a
reliable measurements for snail growth and is widely used by researchers
(Youens and Burks 2007).
3.4.5. Data analyses
For experiment 1 data, we conducted 2-way ANOVAs to test the dependence of
snail shell length and percent mortality on water nutrients, plants, and their
interaction. Residuals for snail mortality were non-normal, primarily due to one
tank with very high mortality (12 of 15 dead) compared to other replicates for that
treatment (0 or 1 dead). To determine if it would be appropriate to exclude or
keep that replicated tank, we conducted a 2-way ANOVA with and without that
51
replicate. Exclusion of that point made the main effects non-significant but the
interaction term significant. We report results with all points included despite the
departure from normality. For experiment 2 data, we conducted a 2-way ANOVA
to test the dependence of snail operculum length on nutrients, plants, and their
interactions. Average snail shell length and operculum length per tank were used
and dead snails were excluded in snail size ANOVAs in experiment 1 and 2. We
conducted a 3-way ANOVA to test the dependence of wet plant mass on snails,
nutrients, plants, and their interactions. In addition, we conducted 2-way
ANOVAs to test the dependence of individual plant species wet mass on
nutrients, snails, and their interactions. Data met the assumptions of ANOVA
(with the exception of snail mortality data). All analyses were conducted in SAS (v 9.4).
3.5. Results
3.5.1. Exp. 1: Nutrient enrichment’s direct and indirect effects on
P. maculata mortality and shell length
Pomacea maculata’s shell length varied with nutrients, plants, and their
interaction (Table 3-1, Appendix Figure 3-1, Figure 3-1a). Snail mortality varied
with plants (Table 3-1, Figure 3-1b). Nutrients or its interaction with plants did not
alter snail mortality (Table 3-1).
52
3.5.2. Exp. 2: Nutrient enrichment effects on P. maculata, plants, and
plant-herbivore interactions
Pomacea maculata operculum length increased with elevated nutrients and
varied with plant identity (Table 3-1, Figure 3-2). The combined effect of nutrient
and plant treatments did not alter snail operculum length (Table 3-1).
Wet plant mass was lower with snails and varied with plant treatments (Table
3-1, Figure 3-3). Nutrients and other factor interactions had no effect on wet plant
mass (Table 3-1). Snails reduced H. umbellata, A. philoxeroides, and
E. crassipes wet mass with no effect on L. spongia wet mass
(Appendix Figure 3-1), Appendix Figure 3-2). Nutrients and its interaction with
snails had no effect on wet plant species masses (Appendix Table 3-1).
3.6. Discussion
Nutrient enrichment increased P. maculata operculum length with no effect on
shell length or native and exotic plant mass. Nutrient enrichment did not alter
snail shell length when snails were fed lettuce, but varied when they were fed
exotic plants in experiment 1, indicating that P. maculata responded to nutrients
indirectly via plants. In addition, nutrient enrichment increased snail operculum
length in experiment 2, suggesting indirect nutrient enrichment effects. Varying
snail shell and operculum length may have been a result of changes in plant
nutritional value or varying plant physical defenses with elevated nutrients, but
our study did not quantify either of these changes. However, studies conducted
on biocontrol herbivores have shown that elevated nutrients increased exotic
53
E. crassipes tissue quality indirectly increasing the performance of biocontrol
grasshopper (Bownes et al. 2013a), a mirid bug (Coetzee et al. 2007), and
weevils (Center and Dray 2010). Furthermore, elevated nutrients may also
change the physical defenses of plants which can then alter the survival, growth,
and reproduction of herbivores. For example, nutrient enriched brown alga Fucus
vesiculosus increased the growth rate, consumption, and reproduction of
herbivorous isopod Idotea baltica by increasing insoluble sugars, reducing total
carbon content, and reducing the physical toughness of the thallus (Hemmi and
Jormalainen 2002), suggesting that nutrient enrichment can alter the nutritional
value and physical defenses of plants. In experiment 1, P. maculata shell length
was greater when they were fed lettuce than when they were fed either
E. crassipes or A. philoxeroides. Similarly, Lach et al. (2000) found that
P. canaliculata grew faster when fed cut lettuce than when fed E. crassipes or
P. stratiotes. In our study, differences in snail shell length with plant identity may
have been a result of varying plant physical defenses. The leaves and stems of
E. crassipes and A. philoxeroides were physically tougher compared to lettuce
leaves, but these differences in plant physical defenses were not quantified.
Because our study did not quantity plant changes with nutrient enrichment and
the length of our studies was not long enough to assess P. maculata’s population
growth or reproduction, longer field studies on several native and exotic plants
that quantify plant changes with nutrient enrichment and that assess the effect of
plant changes on exotic herbivore growth and reproduction are needed.
54
Nutrients did not affect P. maculata mortality but mortality varied with plant
identity in experiment 1. In contrast, survival of native aquatic snail
Potamopyrgus antipodarum varied with nitrogen compound types with ammonia
(96 hour LC50 = 2.02mg/L) being more toxic than nitrite (535mg/L) or nitrate
(1042mg/L) (Alonso and Camargo 2003). However, ammonia levels in our high
nutrient treatments (~0.05mg/L) were lower than those that caused snail mortality
within 96 hours in their study (LC.01 = 0.16mg/L) (Alonso and Camargo 2003). In
addition, a study in the Philippines showed that P. maculata mortality increased
after nitrogen fertilizer was applied (Stuart et al. 2014), but ammonia
concentrations in their study were equivalent to 80 to 400mg/L. These studies
show that nutrient enrichment can have direct negative effects on native and
exotic aquatic snails, but our results suggest that an increase in exotic snail
operculum length with elevated nutrients via native and exotic plants in
experiment 2 may be more important than the direct negative effects of nutrient
levels in eutrophic southeast US waters.
Pomacea maculata reduced overall wet plant mass and wet plant mass
varied with plant species, but plant mass for both exotic plant species was higher
compared to both native species. Another study showed that exotic African snail
(Achatica fulica) and Cuban brown slug (Veronicella cubensis) had varying
effects on native and exotic plants with high damage to some native and some
exotic woody plants, but little damage to other native or exotic species (Shiels et
al. 2014). In addition, a meta-analysis showed that exotic invertebrate herbivores
can reduce native and exotic plant performance, but suggested that this
55
reduction in exotic plant performance would not influence exotic plant invasion
success (Oduor et al. 2010). Higher exotic plant mass independent of snail
presence compared to native plants suggests that exotic plants may survive and
grow under varying biotic environmental conditions, but plant interactions under
varying environmental conditions would need to be assessed to increase our
understanding of plant invasion success. Our results on a limited number of
native and exotic plants suggest caution about drawing inferences about aquatic
plant invasion success based on changes in individual plant species mass with
snails and in no-choice experiments with single plant species because herbivore
feeding preferences and their effects on plant interactions can be complex and
influence exotic plant performance and the their invasion success.
Elevated nutrient enrichment did not alter wet plant mass or individual plant
species masses. In contrast, other studies have shown significant effects of
elevated nutrients on plant performance. For instance, nutrient enrichment
affected native and exotic grasses in a fertilization experiment in western North
American grasslands but its effect did not depend on plant origin (Seabloom et
al. 2011). There is evidence that elevated nutrients increase plant mass with a
general pattern of higher exotic plant productivity compared to native plants in
deserts (Brooks 2003), grasslands (Huenneke et al. 1990), salt marshes (Tyler et
al. 2007), and marine habitats (Gennaro and Piazzi 2014). A model also
predicted that elevated nutrients can increase E. crassipes growth ten-fold
(Wilson et al. 2005), suggesting that this may be one exotic aquatic plant species
that may invade more readily with elevated nutrients. These studies show that
56
elevated nutrients increase plant productivity with greater effects on exotic plants
in many ecosystems, but our study does not support those findings. We might
not have been able to detect an increase in native and exotic plant mass with
elevated nutrients with greater effects on exotic plants for several reasons that
include the length of study, numbers of plant species included (single vs. many),
type of study (greenhouse vs. field), time of the year when study was conducted,
or nutrients may not have been limiting under greenhouse conditions. To
increase our understanding of nutrient enrichment effects on native and exotic
plants and their effects on exotic herbivores, longer field studies that include
several native and exotic plants individually and in combination are needed.
In conclusion, these studies suggest that freshwater wetland ecosystems may
become readily invaded by exotic herbivores and multiple exotic plants. Nutrient
enrichment may increase the probability of P. maculata invasions in aquatic
ecosystems by increasing snail growth, potentially reducing time to reach
reproductive maturity as has been suggested for P. canaliculata (Lach et al.
2000) that could increase their reproduction, growth rate, and spread to
neighboring eutrophic habitats. Snails reduced exotic plants mass, but exotic
plant mass was greater than native plants independent of snail presence,
suggesting that these plants may survive and grow in habitats with varying biotic
environmental conditions, but studies evaluating both plant and plant-herbivore
interactions are needed. Together these results suggest that nutrient enrichment
may increase the probability of multiple plant and herbivore invasions in
freshwater wetland ecosystems.
57
3.7. Acknowledgments
We thank Erika Soltero for her assistance in the lab and Romi Burks, Jenn
Rudgers, Amy Dunham, Volker Rudolf, and Anna Armitage for helpful
discussions. This work was supported by an AGEP-Rice University Fellowship
(to MML) and a Ford Foundation Predoctoral Fellowship (to MML).
Table 3-1 The dependence of exotic P. maculata snail shell length and percent mortality in experiment 1 and
P. maculata operculum length and wet plant mass in experiment 2 on nutrients, plants, snails, and their
interactions in ANOVAs. Significant results are shown in bold
Experiment 1
Snail shell
length
Factor
df
Fx,36
P
Experiment 2
Snail %
mortality
Fx,36
P
Snail
operculum length
df
Fx,34
P
Wet plant
mass
df
Fx,72
P
Nutrients
2
15.2
<0.0001
0.1
0.9430
2
71.5
< 0.0001
2
0.9
0.3939
Plants
2
1,361.4
<0.0001
3.4
0.0449
3
3.0
0.0432
3
79.2
< 0.0001
Nutrients*plants
4
11.5
<0.0001
1.3
0.2724
6
2.0
0.0954
6
1.1
0.4019
Snails
1
30.0
<0.0001
Snails*nutrients
2
1.0
0.3819
Snails*plants
3
2.1
0.1041
Snails*nutrients*plants
6
1.0
0.4170
58
59
25
a
a
a
Nutrients
Control
Low
High
a
20
15
cd
10
b
b bc
d
e
5
0
20
P. maculata % mortality
P. maculata shell length (mm)
30
b
a
15
10
ab
5
b
0
Lettuce
E. c.
A. p.
Plants
Lettuce
E. c.
A. p.
Plants
Figure 3-1 The dependence of exotic P. maculata (a) shell length on nutrients and plants and (b) percent mortality
on plant species in experiment 1. Means+1SE. Means with the same letter were not significantly different in
post-hoc tests. E. c. = E. crassipes and A. p. = A. philoxeroides
P. maculata operculum length (mm)
12
a
b
a
b
8
c
4
0
Control
Low
Nutrients
High
L. s.
H. u.
A. p.
E. c.
Plants
Figure 3-2 The dependence of exotic P. maculata operculum length on (a)
nutrients and (b) plants in experiment 2. Means +1SE. Means with the same
letters were not significantly different in post-hoc tests. L. s. = L. spongia,
H. u. = H. umbellata, A. p. = A. philoxeroides, E. c. = E. crassipes
60
a
b
a
Wet plant mass (g)
40
30
a
b
20
b
c
10
d
0
No snails
Snails
Snails
L. s.
H. u.
A. p.
E. c.
Plants
Figure 3-3 The dependence of wet plant mass on (a) snails and (b) plants in
experiment 2. Means +1SE. Means with the same letters were not
significantly different in post-hoc tests. L. s. = L. spongia,
H. u. = H. umbellata, A. p. = A. philoxeroides, E. c. = E. crassipes
61
Chapter 4
Nutrient enrichment effects on invasions
depend on climate warming: an
experimental test with freshwater
wetland plant communities
4.1. Abstract
Anthropogenic environmental change can increase species invasions and reduce
native biodiversity. Nutrient enrichment may favor exotic plant species that
typically have higher growth rates. Warming may increase the performance of
pre-adapted exotic species from warmer native ranges and/or decrease the
performance of locally adapted native species. However, the community level
impacts of nutrient enrichment and warming will depend on their combined
effects on individual species and their interactions. We conducted an 11-month
field experiment with freshwater wetland plant communities in 474L tanks in
62
63
Houston, TX that manipulated 1) plant community composition: native plants
[4 species], exotic plants [3 species from warm, nutrient rich habitats], or both
native and exotic plants [7 species]; 2) nutrients: ambient or high (+6mg/L
Nitrogen and +1.7mg/L Phosphorus); and 3) temperature: ambient, +1°C, or
+2°C in a factorial design. Elevated nutrients increased plant mass, favored
exotic plants, and increased exotic plant diversity. Exotic plants reduced native
plant diversity and reduced native plant mass in elevated nutrients. Elevated
nutrients increased (2 exotic species) or decreased (1 exotic species, 3 native
species) species’ relative abundance but for the majority of species the
magnitude of these changes depended on warming. These results suggest that
nutrient enrichment may increase invasions by some exotic plants but warming
will modify the magnitude of these effects. In addition, warming will influence the
particular exotic plant species that dominate invasions with nutrient enrichment
and the native species that will be most heavily impacted in freshwater wetland
ecosystems.
4.2. Keywords
warming, nutrient enrichment, Alternanthera philoxeroides, Eichhornia crassipes,
Pistia stratiotes, freshwater mesocosms
4.3. Introduction
Anthropogenic factors can contribute to species invasions and reduce native
biodiversity (Stevens et al. 2004; Walther 2010; Cockrell and Sorte 2013) and
64
generate novel communities (Hobbs et al. 2006; Williams and Jackson 2007).
Researchers have emphasized the need to investigate the interactive effect of
multiple anthropogenic factors on native and exotic species performance
(Didham et al. 2007; Crain et al. 2008; Bradley et al. 2010; Dukes et al. 2011)
and species interactions (Tylianakis et al. 2008; van der Putten et al. 2010;
Gennaro and Piazzi 2011; Verlinden et al. 2014). Many studies have investigated
the effect of individual anthropogenic factors on species performance (Tyler et al.
2007; Henry-Silva et al. 2008; Cockrell and Sorte 2013; Gennaro and Piazzi
2014) but only a few studies have investigated the effects of multiple
anthropogenic factors on exotic species (Crain et al. 2008; Dukes et al. 2011;
Griffiths et al. 2014; You et al. 2014).
Nutrient enrichment typically increases plant growth, but often has larger
positive effects on exotic plant performance compared to native plants,
increasing exotic plant dominance and success in invaded habitats (Rickey and
Anderson 2004; Tyler et al. 2007). Nutrient enrichment may favor exotic plants
because some of the exotic plants possess characteristics that include rapid
growth rates and high phenotypic plasticity which allows them to quickly take
advantage of available resources. For instance, elevated nutrients increased
native riparian species and Arundo donax mass, but favored A. donax (Quinn et
al. 2007). In addition, these characteristics make exotic plants suitable
candidates for wastewater remediation because they can efficiently remove
nutrients from enriched water. Some of the exotic plants used in remediation
include Eichhornia crassipes, Pistia stratiotes, and Alternanthera philoxeroides
65
(Boyd 1970; Jayaweera and Kasturiarachchi 2004; Rodríguez-Gallego et al.
2004; Lu et al. 2010). These subtropical exotic plants might also be used for
wastewater remediation because they originate from aquatic ecosystems with
high water nutrient levels (Roberto et al. 2009).
Warming effects on exotic species have been investigated using various
methods including climate based models (e.g. CLIMEX) that assess exotic
species habitat suitability and potential species distributions in the introduced
range (Ramsfield et al. 2007; Kriticos et al. 2007; Potter et al. 2009) and
experiments that evaluate the effect of warming on exotic species performance
(Dukes et al. 2011). Climate based models predict how warming may influence
exotic species distribution by comparing the climate in the native and the
introduced range of exotic species or by quantifying changes in the distribution of
exotic species at a particular location over time. Climate based models that
compare climatic conditions in the native and introduced range of exotic species
are limited because they primarily focus on the range of tolerance of exotic
species. Furthermore, climate based models often predict wider species
distributions than what is observed because they do not consider the effect of
dispersal, species interactions, or the interaction of warming with other
anthropogenic factors (Davis et al. 1998a; Wharton and Kriticos 2004).
Warming effects via changes in maximum, minimum, and average
temperatures may alter the distribution of exotic species by altering the length of
the growing season which may affect exotic species survival, growth, and
reproduction. Furthermore, warming may alter the outcome of native and exotic
66
species interactions, altering community composition patterns if native and exotic
plant responses to warming vary in direction or magnitude (Davis et al. 1998b;
Dukes and Mooney 1999; Rahel and Olden 2008; Walther et al. 2009). For
example, experimental warming increased exotic yellow star thistle’s growth and
abundance with no effect on native plants, suggesting that warming may favor
those exotic plants (Dukes et al. 2011). In contrast, experimental warming with
temperatures above 30°C reduced the growth rate of native Azolla filiculoides
and Lemna minor and exotic Salvia molesta, suggesting that warming can have a
negative effect on both native and exotic plants (van der Heide et al. 2006b).
However, warming may increase the performance of exotic subtropical plants
such as E. crassipes, P. stratiotes, and A. philoxeroides that are sensitive to cold
temperatures, hard freezes, and ice cover (Owens and Madsen 1995; Li et al.
2012). These studies show varying effects of warming on native and exotic
plants, suggesting that additional studies are needed to increase our
understanding of warming effects on exotic species and their effect on native
species.
Eichhornia crassipes (water hyacinth - Pontederiaceae) is considered one of
the worst aquatic weeds in the world with high socio-economic and ecological
impacts (Lowe et al. 2004). It was intentionally introduced from South America to
the USA in 1884, invaded southern USA states by the 1900’s, and it currently
invades more than 50 countries on five continents (Lowe et al. 2004). The
optimum temperature for E. crassipes growth is 28-30°C. A CLIMEX model
showed that southern United States is suitable habitat for E. crassipes (Brunel
67
2012). In addition, a study showed that low temperatures ranging from 5-8°C
reduced the regrowth potential of E. crassipes, changing its distribution (Owens
and Madsen 1995). Furthermore, winter temperatures in the Great Lakes
reduced E. crassipes winter survival (Rixon et al. 2005), influencing population
growth and infestation during the growing season. However, warming may allow
E. crassipes to overwinter in the Great Lakes. Eichhornia crassipes has been
observed in various locations with air and water temperatures between 8-10°C
and 10-11°C (Adebayo et al. 2011). In addition, experimental warming in the
winter increased E. crassipes’ survival and clonal reproduction (You et al. 2013).
Pistia stratiotes (water lettuce - Araceae) is on the list of the World’s Worst
Weeds (Evans 2013). It was introduced from South America to the United States,
likely accidentally, and was first reported in Florida in 1765 (Stuckey and Les
1984). It is currently found in Europe, Africa, and Asia (Neuenschwander et al.
2009). The optimum temperature for P. stratiotes growth is 22-30°C. A study
showed that freezing temperatures in South Florida increased P. stratiotes’
winter mortality, suggesting that P. stratiotes is sensitive to low temperatures
(Dewald and Lounibos 1990). Warming may increase the distribution of
P. stratiotes by increasing temperature during winter. Pistia stratiotes has been
able to overwinter in a natural thermal stream in Topla in Slovania that has water
temperature above 17°C all year (Šajna et al. 2007) and in ponds with warm
water discharges in the winter (Kadono 2004; Tamada et al. 2015).
Alternanthera philoxeroides (alligator weed- Amaranthaceae) was
accidentally introduced from the Parana River region of South America (Julien et
68
al. 1995). In the United States, it was first recorded in Mobile, Alabama in 1897
and invaded coastal states from North Carolina to Texas by 1963 (Spencer and
Coulson 1976). The optimum temperature for A. philoxeroides growth is 15-20°C.
Shorter growing seasons and a higher number of frost events at higher latitudes
have been shown to kill the top growth of A. philoxeroides, reducing its mass
accumulation during the growing season (Julien et al. 1992). A climate based
model using distribution data from the native range of A. philoxeroides showed
that the southern United States is suitable habitat for A. philoxeroides (Julien et
al. 1995). However, an experimental study showed that warming effects on
A. philoxeroides depend on the plant’s physical characteristics. Warming reduced
the growth of A. philoxeroides fragments that had connected stolons but
increased growth of fragments with severed stolons (Li et al. 2012). Warming in
Houston may benefit these exotic plants by reducing frost events that may
reduce winter mortality and increase mass accumulation during the growing
season.
Species interactions may alter the effect of warming on species with other
anthropogenic factors influencing the effects of warming. For instance, warming
increased exotic Solidago gigantea dominance when it was planted with native
Plantago lanceolata, but reduced the dominance of S. gigantea when planted
with native Epilobium hirsutum (Verlinden et al. 2014). In addition, nitrate
reduced exotic Centaurea solstitialis establishment in ambient temperature, but
increased its establishment with warming (Dukes et al. 2011). Furthermore,
nutrient enrichment together with warming increased the growth and clonal
69
propagation of E. crassipes in China (You et al. 2014). Studies investigating the
interactive effect of multiple anthropogenic factors on exotic species are
increasing, but our understanding of how plant interactions alter the effect of
anthropogenic factors on species invasions and their impact on native species
remain limited (Didham et al. 2007).
Here, we investigated the individual and interactive effects of nutrient
enrichment and warming on plant invasions in native freshwater wetland plant
communities and their effect on native plants with a field mesocosm experiment.
4.4. Methods
4.4.1. Study system
Alternanthera philoxeroides, E. crassipes, and P. stratiotes heavily invade
wetlands in southeast Texas. These plants are sympatric in their native range
(South America) and co-occur in the introduced range with native wetland plants
that include Hydrocotyle umbellata (water pennywort - Araliaceae), Limnobium
spongia (frog's bit - Hydrocharitaceae), Pontederia cordata (pickerelweed Pontederiaceae), Typha latifolia (cattail - Typhaceae), and native snails Physa
acuta (bladder snail - Physidae) and Planorbella trivolvis (marsh ramshorn snail Planorbidae). We selected plants in this study based on their functional
characteristics. Native H. umbellata, T. latifolia, P. cordata and exotic
A. philoxeroides are emergent plants. Hydrocotyle umbellata and
A. philoxeroides can grow in both terrestrial and aquatic habitats. Exotic
E. crassipes, P. stratiotes, and native L. spongia are free-floating aquatic plants
70
with clonal reproduction. Eichhornia crassipes and L. spongia have similar plant
structure. Furthermore, P. cordata and E. crassipes belong to the same family.
Alternanthera philoxeroides in aquatic habitats anchors to banks and
reproduces clonally with no viable seeds in its introduced range (Spencer and
Coulson 1976; He et al. 2014). It can form large interwoven mats or free-floating
monocultures from stem fragments because the hollow stems can float and root
at the nodes (Spencer and Coulson 1976; Sainty et al. 1997). Eichhornia
crassipes reproduces clonally and has free-floating rosettes. Newly formed
rosettes can break easily, allowing E. crassipes to disperse and colonize
neighboring habitats. Similarly, P. stratiotes is characterized by free-floating
rosettes that can exist on their own or as interconnected clones forming
free-floating mats.
4.4.2. Experimental setup
To investigate the individual and interactive effect of nutrient enrichment and
warming on native and exotic plants and their interactions, we conducted a
3×2×3 factorial mesocosm experiment that manipulated 1) plant composition:
native plants only (H. umbellata, L. spongia, P. cordata, and T. latifolia), 2) exotic
plants only (A. philoxeroides, E. crassipes, and P. stratiotes) or both (four native
and three exotic plant species), 2) nutrients: control (ambient) or high
(+6mg/L Nitrogen and +1.7mg/L Phosphorus), and 3) temperature: ambient,
+1°C, or +2°C with four replicates per treatment.
In May 2012, we set up 72 mesocosms by adding 15cm of topsoil/sand
mixture and water to 454L tanks at the Rice University South Campus Field
71
Station. We added an individual of each of the four native plant species to tanks
assigned to native plant only communities. We added an individual of each of
three exotic plant species to tanks assigned to exotic plant only communities. We
added approximately 160g of fresh plant mass to each of these tanks. We added
an individual of each of the four native and an individual of each of the three
exotic plant species to the tanks with both groups (~ 320g of fresh plant mass).
We replaced plants that did not survive at least two weeks after the initial planting
with a new individual of equivalent mass. After two weeks, we added 40 native
P. acuta and P. trivolvis snails to all mesocosms to reduce snail variation among
plant communities (because they are often accidentally introduced to
mesocosms). We selected nutrient levels based on nutrient levels in southeast
Texas wetlands. To deliver the randomly assigned nutrient and temperature
water treatments to each community, we setup a flow-through watering system
with drip emitters in each tank that resulted in a four-day hydraulic residence
time. We mixed a soluble fertilizer (28-8-18) with municipal water in a holding
tank that was then added into the water lines for the elevated nutrient treatments
with a fertilizer injector (Dosatron) and then delivered to communities. To achieve
temperature treatments, we passed water through zero (ambient), two (+1°C), or
four (+ 2°C) solar water heaters (each 1.2 x 6 m, Specialty Pool Products, East
Windsor CT, USA) before being delivered to communities. We supplemented
solar water heaters with electric water heaters (four 1800 watt heaters, SR-15L,
Chronomite, City of Industry CA, USA) during the winter months due to low solar
radiation. We conducted monthly visual plant surveys to estimate plant cover by
72
species. After 11 months, we harvested aboveground plant mass that was sorted
by species, oven-dried, and weighed.
4.4.3. Data analyses
We used ANOVAs to test the dependence of plant mass and diversity (Shannon
Diversity Index) on plant composition, nutrients, temperature, and their
interactions. We conducted repeated measures ANOVAs to test the dependence
of percent cover on community composition, nutrients, temperature, and their
interactions. We excluded native plant only communities from exotic plant
analyses and exotic plant only communities from native plant analyses. We
conducted repeated measures ANOVAs on species’ proportional cover in
communities with both native and exotic plants to test their dependence on
nutrients, temperature, and their interactions. Data met the assumptions of
ANOVA and repeated measures ANOVA. We conducted post-hoc tests to
determine the differences between treatment levels for significant variables with
more than two levels. We also conducted PERMANOVAs to examine community
variation in native plant only, exotic plant only, and communities with both native
and exotic plants in relation to nutrients, temperature, and their interaction using
plant mass. We performed all ANOVAs using SAS (v 9.4) and PERMANOVAs
using R (v 3.2.0). We conducted NMS ordinations using mass by species to
examine variation in native plant only, exotic plant only, and communities with
both native and exotic plants in relation to nutrients, temperature, and their
interaction (PCord4, 500 iterations, Sorensen [Bray-Curtis] distance, 2 initial
axes, 0.01 step-down threshold, 0.005 stability criterion). In addition, we
73
predicted exotic to native plant mass ratios from native plant only and exotic plant
only communities and compared it to the observed exotic to native plant mass
ratio in plant communities with both native and exotic plants. The predicted exotic
to native plant mass ratio was obtained by randomly pairing exotic and native
plant masses from native plant only and exotic plant only communities
(5000 times, without replacement).
4.5. Results
Native plant only, exotic plant only, and communities with both native and exotic
plants varied in relation to nutrients but were not influenced by temperature or
their interaction (Table 4-1, Figure 4-1). Elevated nutrients increased native plant
mass and native plant mass was higher in native plant only communities
(Table 4-2, “nutrients”, “composition*nutrients”, Figure 4-1b,1d, Figure 4-3a).
Other factors and their interactions did not affect native plant mass (Table 4-2).
Native plant diversity depended on community composition and on nutrients
(Table 4-2, Figure 4-3a). Temperature and factor interactions did not affect native
plant diversity (Table 4-2). Exotic plant mass depended on community
composition, nutrients, and their interaction (Table 4-2, “nutrients”,
“composition*nutrients”, Figure 4-1a,1c, Figure 4-3c). Temperature and other
factor interactions did not affect exotic plant mass. Elevated nutrients increased
exotic plant diversity independent of community composition, temperature, and
their interactions (Table 4-2, “nutrients”, Figure 4-3c-d).
74
Native plant percent cover varied with community composition, nutrients, and
their interaction (Appendix Table 4-1). Temperature and other factor interactions
did not affect native plant percent cover (Appendix Table 4-1). Elevated nutrients
increased exotic plant percent cover independent of community composition,
temperature, and their interaction (Appendix Table 4-1, “nutrients”, Figure 4-2).
In most cases, the expected exotic to native plant mass ratio was significantly
higher than in communities with both native and exotic plants with the exception
of ambient nutrients and in +1°C treatments (Table 4-3). Elevated nutrients
increased native P. cordata and T. latifolia mass with no effect on H. umbellata
(Appendix Figure 4-1g,n,k; respectively). Limnobium spongia’s mass varied with
community composition, nutrients, and their interaction (Appendix Figure 4-1i-j).
Elevated nutrients increased L. spongia’s mass in native plant only communities
(Appendix Figure 4-1i, Appendix Figure 4-2a). Temperature and other factor
interactions did not affect the mass of native species (Appendix Figure 4-1g-n).
Eichhornia crassipes’ mass varied with community composition, nutrients, and
their interaction (Appendix Figure 4-1). Elevated nutrients increased E. crassipes’
mass in exotic plant only communities (Appendix Figure 4-2b). Elevated nutrients
increased exotic A. philoxeroides’ mass but had no effect on P. stratiotes’ mass
(Appendix Figure 4-1c,e). Temperature and other factor interactions did not affect
E. crassipes, A. philoxeroides, and P. stratiotes’ mass (Appendix Figure 4-1a-f).
Elevated nutrients increased proportional plant cover of exotic P. stratiotes and
E. crassipes and reduced proportional plant cover of exotic A. philoxeroides and
native P. cordata, L. spongia, and T. latifolia (Table 4-4). Elevated nutrients had
75
no effect on H. umbellata and warming reduced P. cordata’s proportional plant
cover (Table 4-4). Furthermore, warming reduced the effect of elevated nutrients
on E. crassipes’ proportional plant cover (Table 4-4). Warming with elevated
nutrients increased H. umbellata’s proportional plant cover (Table 4-4). Warming
increased L. spongia’s proportional plant cover in ambient temperature
treatments (Table 4-4).
4.6. Discussion
Nutrient enrichment increased exotic plant invasions but warming influenced the
magnitude of nutrient enrichment effects on exotic species. Variation in species’
responses to nutrient enrichment and warming suggest that these effects are
species specific results of plant characteristics including growth rate. For
instance, exotic E. crassipes and native L. spongia had similar responses to
nutrient enrichment and warming possibly because both have similar phenotypes
and growth forms. They also grow rapidly with elevated nutrients, allowing them
to take advantage of available resources possibly outcompete other species in
the community. A study conducted in China also found that the growth, clonal
reproduction, and shoot/root ratio of E. crassipes increased with nutrient
enrichment and with warming but without an interactive effect (You et al. 2014).
Nutrient enrichment favored exotic plants increasing plant invasion success
but these effects were greater for exotic plants in exotic plant only communities
than for exotic plants in communities with both native and exotic plants. Other
studies have shown that competition with native plants can reduce the positive
76
effects of nutrient enrichment on exotic plants. For instance, elevated nutrients
increased exotic Centaurea solstitialis mass in monoculture but had no effect on
C. solstitialis mass when grown with native Avena barbata (Dukes et al. 2011). In
addition, exotic Acacia saligna outperformed native Protea repens in elevated
nutrient conditions, but their performance was equivalent when grown together in
low nutrient conditions (Witkowski 1991). In our study, native T. latifolia and
exotic E. crassipes were the dominant species in communities with both native
and exotic plants. These species could have reduced each other’s performance
and that of other species because both have rapid growth rates that allow them
to take advantage of available resources. Even though native T. latifolia had
higher mass than L. spongia in our study, it is possible that L. spongia had a
greater effect on E. crassipes’s invasion compared to T. latifolia because
L. spongia and E. crassipes have similar phenotypes and growth rates. Both
have low stature in ambient or low nutrient conditions and elongated petioles and
broader leaves in elevated nutrient conditions. They are also often mistaken for
one another in the field because they look very similar to each other especially in
high nutrient water habitats. Furthermore, higher predicted exotic to native plant
mass ratio from native plant only or exotic plant only communities than in
communities in which they co-occurred suggests that it is necessary to
investigate effects of multiple anthropogenic factors at the community level to
understand their effects on plant invasions and their combined impact on native
species.
77
Nutrient enrichment increased plant invasion success overall but not all exotic
plants benefitted from elevated nutrients. Althernanthera philoxeroides was the
most abundant exotic plant in ambient nutrient conditions, suggesting that it may
be a more problematic invader in low resource habitats. Another study, showed
that E. crassipes may survive in ambient nutrient conditions but requires
abundant nitrogen, phosphorus, and potassium to grow (Rodríguez-Gallego et al.
2004). Only some species had positive responses to nutrients, perhaps due to
variation in their characteristics. Our results show that exotic plant mass varied
with nutrient enrichment and suggest that exotic species’ mass is not always
higher than native species’ mass under the same environmental conditions in
similar conditions. Exotic species performance may be higher, lower, or
equivalent to the performance of native species depending on species identity
and environmental conditions (Daehler 2003). Furthermore, we expected
elevated nutrients to reduce exotic plant diversity because some of these exotic
plants have higher growth rates that may result in an increase in competitive
ability, potentially excluding slow growing plants. In our study, elevated nutrients
increased exotic plant diversity because more species were abundant with
elevated than with ambient nutrients. It is possible that fewer exotic plants
persisted in ambient nutrient conditions because these exotic plants are
preadapted to nutrient rich water in their native range (Roberto et al. 2009). Our
results suggest that nutrient poor habitats may be less susceptible to plant
invasions and that nutrient rich habitats will increase the probability of multiple
plant invasions in aquatic ecosystems.
78
We expected warming to increase plant invasions but instead it had no effect
on plant invasions. We expected exotic plants to be closer to their optimum
climatic conditions during the growing season with warming and to have lower
winter mortality and higher exotic plant regrowth and mass accumulation during
the growing season with an increase in winter temperatures. However, we might
not have detected an effect of warming in Houston because winter temperatures
were mild, suggesting that it may not have had an effect on winter plant mortality.
In addition, climate based models predict that areas in Houston where
E. crassipes and A. philoxeroides occur are already suitable habitats for these
species (Julien et al. 1995), suggesting that an increase of 1°C to 2°C in Houston
will not affect plant invasions but may influence the effect of nutrient enrichment
on some exotic species. Furthermore, the length of the study may not have been
long enough to quantify warming effects on exotic plant regrowth and mass
accumulation during the growing season. Other studies have shown that
warming may have positive and negative effects on plant invasions (Bradley et
al. 2010). For instance, De Sassi et al. (2012) showed that warming reduced
native species richness and increased exotic plant abundance. Warming may
increase plant invasions by increasing exotic species growth rates in areas that
are already suitable for the species or by reducing winter mortality closer to their
northern range of distribution as predicted by climate based models. In contrast,
warming reduced the growth of exotic plants in an Australian temperate
grassland relative to native plant growth (Williams et al. 2007). Warming may
also reduce exotic plant performance when its maximum temperature tolerance
79
is reached. These studies show that warming may have opposing effects on
plant invasions; therefore additional field studies that use information from
climate based models are necessary to increase our understanding of the
mechanisms by which warming may affect plant invasions and exotic species
performance throughout their predicted distribution range and their effect on
native communities.
In conclusion, nutrient enrichment will likely increase plant invasions in these
ecosystems but the magnitude of this effect on exotic species likely depends on
warming. Elevated nutrients increased exotic plant mass and diversity, increasing
the probability of multiple plant invasions in invaded habitats. However, nutrient
enrichment effects on plant invasions based on exotic plant only communities
overestimated the actual effects in communities with both native and exotic
plants. In addition, warming had no effect on plant invasions possibly because
these exotic species already occur in habitats with suitable climatic conditions as
predicted by climate based models. However, it did increase the relative
abundance of some exotic species. Therefore, additional experimental studies
that use information from climate based models are necessary to increase our
understanding of the mechanism by which nutrient enrichment and warming
affect plant invasions and their combined effect on native communities.
4.7. Acknowledgements
We thank: Candice Tiu, Qiang Yang, Peter Sylvers, Jordan Bunch, Daniel
McDermott, Abby Lamb, Cassandra Corrales, Dana Galvan, Michelle Shapiro,
80
Sarah Margolis, Ariel Nixon, Ling Zhang, and Gang Liu for their assistance in the
field; Romi Burks, Amy Dunham, Volker Rudolf, and Anna Armitage for helpful
discussions. This work was supported by a Ford Foundation Predoctoral
Fellowship (to MML), an Environmental Protection Agency Science to Achieve
Results Fellowship for Graduate Environmental Study (to MML), a Rice
University Shell Center for Sustainability research grant (to MML), and a Rice
centennial award to support undergraduate research (to MML).
81
Table 4-1 The dependence of community composition using plant mass in native plant only, exotic plant only,
and communities with both native and exotic plants on nutrients, temperature, and their interaction in
PERMANOVAs. Significant results are shown in bold
Native only
Factor
Nutrients
Temperature
Nutrients*temperature
Exotic only
Native + Exotic
DF Pseudo-Fx,18 P(perm) Pseudo-Fx,18 P(perm) Pseudo-Fx,18 P(perm)
1
2
2
36.0
2.0
2.2
0.0002
0.1152
0.0872
57.6
0.7
0.6
0.0002
0.2482
0.3202
22.5
0.7
0.6
0.0002
0.6164
0.6914
Table 4-2 The dependence of native and exotic plant mass and diversity (Shannon Diversity Index) on plant
composition, nutrients, temperature, and their interactions in ANOVAs. Significant results are shown in bold
Native mass
Factor
DF Fx,36
2.6
P
Native diversity
F x,36
P
Exotic mass
F x,36
Composition
1
0.1152
9.5
0.0039
6.5
Nutrients
1 90.4 <0.0001
18.0
0.0001
Temperature
2
1.7
0.1903
1.2
0.3297
2.4
Composition*nutrients
1
5.2
0.0280
2.0
0.1616
Composition*temperature
2
0.1
0.8904
2.5
Nutrients*temperature
2
0.8
0.4711
Composition*nutrients*temperature
2
1.0
0.3711
P
Exotic diversity
F x,36
P
0.0153
3.4
0.0730
90.8 <0.0001
18.8
0.0001
0.1079
0.5
0.6140
6.5
0.0153
2.9
0.0978
0.0957
0.5
0.6131
1.2
0.3051
1.7
0.1950
2.3
0.1128
0.1
0.9479
0.5
0.6169
0.5
0.5965
0.1
0.5835
82
83
Table 4-3 The dependence of exotic to native plant mass ratio on nutrients,
temperature and their interaction, in contrasts of expected ratio from native
only and exotic only plant communities and the observed ratio from
communities with both native and exotic plants. Significant results are
shown in bold
Contrast
Expected Observed
P
All communities
0.37
0.28
0.0080
Ambient nutrients
High nutrients
+0°C
+1°C
+2°C
Ambient nutrients,
+0°C
High nutrients, +0°C
Ambient nutrients,
+1°C
High nutrients, +1°C
Ambient nutrients,
+2°C
High nutrients, +2°C
0.07
0.45
0.50
0.34
0.29
0.06
0.36
0.36
0.35
0.16
0.1500
<0.0001
<0.0500
0.1200
<0.0001
0.09
0.06
0.0400
0.56
0.48
0.0400
0.05
0.08
0.0400
0.45
0.44
0.0400
0.06
0.04
0.0400
0.34
0.20
0.0400
84
Table 4-4 The dependence of species cover on nutrients, temperature, and
their interactions in repeated measures ANOVAs using proportional cover
for each species in communities with both native and exotic plants.
Significant results are shown in bold
Repeated measures
Species
Nutrients
F1,18
Exotic
A.
alligator
79.7
philoxeroidesweed
water
E. crassipes
236.4
hyacinth
P. stratiotes water lettuce 17.8
Native
T. latifolia
cattail
29.4
L. spongia frog’s bit
96.7
water
H. umbellata
2.9
pennywort
P. cordata pickerelweed 29.5
Temperature
Nutrients
*temperature
F2,18
P
P
F2,18
P
<0.0001
0.2
0.8014
0.9
0.4094
<0.0001
4.3
0.0301
3.9
0.0404
0.0005
1.9
0.1746
2.8
0.0873
<0.0001
<0.0001
2.9
4.1
0.0827
0.0338
1.4
6.3
0.2636
0.0085
0.1034
6.7
0.0066
6.4
0.0080
<0.0001
3.7
0.0467
2.3
0.1255
85
25
a. exotics only
b. natives only
0.6
20
0.3
Axis 2
Rank
15
10
+0C - control
+1C - control
+2C - control
+0C + NP
+1C + NP
+2C + NP
5
0
-0.3
1 kg
2 kg
4 kg
-0.6
1.0
1.0
c. native + exotic
[exotic mass]
0.5
d. native + exotic
[native mass]
0.5
Axis 2
Axis 2
0.0
0.0
-0.5
0.0
-0.5
-1.0
-1.0
-1
0
Axis 1
1
2
-1
0
1
2
Axis 1
Figure 4-1 The dependence of plant mass in communities with (a) exotic
plants only or (b) native plants only ,and (c) exotic plant mass and (d)
native plant mass in communities with both native and exotic plants.
86
Percent cover (average over 11 months)
120
100
80
60
Native
T. latifolia
L. spongia
H. umbellata
P. cordata
Exotic
A. philoxeroides
P. stratiotes
E. crassipes
40
20
0
ol
ol
ol
i gh
i gh
i gh
contr
contr
contr
C-h
C-h
C-h
0
1
2
C
C
+
+
+
C
2
+
+0
+1
Temperature - nutrients
Figure 4-2 The dependence of percent cover for each native and exotic
plant species on temperature and nutrients in communities with both
native and exotic plants
87
(a)
(b) 0.8
a
4
b
3
2
c
c
a
Native diversity
Native mass (kg)
5
Nutrients
control
high
b
0.6
0.4
0.2
1
0.0
0
np
np+ ep
(c)
np + ep
ep
np + ep
4
a
3
2
b
Exotic diversity
Nutrients
control
high
5
Exotic mass (kg)
np
(d) 0.8
0.6
0.4
0.2
1
c
c
0.0
0
ep
np + ep
Community composition
Community composition
Figure 4-3 The dependence of (a-b) native and (c-d) exotic plant mass and
diversity on nutrients and community composition. Means +1SE. Means
with the same letters were not significantly different in post-hoc tests.
Np = native plant, ep = exotic plant, np + ep = native and exotic plants in
community
88
Chapter 5
Warming increased exotic snail
reproduction independent of nutrient
enrichment and plant invasions in
wetland communities
5.1. Abstract
Anthropogenic factors can contribute to multiple plant and animal invasions in
invaded ecosystems. Climate warming and nutrient enrichment individually and
in combination may affect plant and herbivore invasions directly or impact
invasions by changing plant-herbivore interactions. To investigate warming and
nutrient enrichment effects on plant and snail invasions and their effect on native
plant and snail communities, we established forty freshwater wetland
communities with native plants and snails that were then invaded by an exotic
snail and assigned to three treatments in a factorial design: 1) native or exotic
89
plant addition, 2) control (no addition) or elevated nutrients [+6mg/L Nitrogen and
+2mg/L Phosphorus], and 3) ambient or +2°C temperature. Warming did not
affect plants but increased exotic snail reproduction four-fold. Nutrient enrichment
and warming increased exotic snail mass resulting in an increase in snail
reproduction and population growth rates by reducing the time needed for snails
to reach reproductive maturity. Elevated nutrients also increased plant mass and
native snail abundance. However, exotic plant mass was higher than native plant
mass, suggesting that nutrient enrichment will increase the likelihood of plant
invasions. In addition, exotic plants reduced native plant mass while elevated
nutrients and warming had no effect on native plant mass. Our results suggest
that warming with elevated nutrients could increase the likelihood of aquatic
herbivore invasions and that nutrient enrichment could enhance the effect of
exotic plants on native plants in freshwater wetland communities.
5.2. Keywords
warming, nutrient enrichment, Pomacea maculata, Alternanthera philoxeroides,
Eichhornia crassipes, Pistia stratiotes, wetland communities, mesocosms
5.3. Introduction
Many anthropogenic factors are known to contribute to species invasions that
decrease native biodiversity (Stevens et al. 2004; Walther 2010; Cockrell and
Sorte 2013) and generate novel communities (Hobbs et al. 2006; Williams and
Jackson 2007). Researchers have repeatedly emphasized the need to
90
investigate the interactive effect of multiple anthropogenic factors on exotic
species and species interactions (Gritti et al. 2006; Scherer-Lorenzen et al. 2007;
Didham et al. 2007; Tylianakis et al. 2008; Crain et al. 2008; van der Putten et al.
2010; Griffiths et al. 2015) to better predict species invasions and increase our
understanding of the effects of multiple anthropogenic factors on exotic species
and their effect on native ecosystems. Anthropogenic factors such as warming
and nutrient enrichment may increase the probability of plant and consumer
invasions based on studies that have investigated their individual effects (Wilson
et al. 2005; Quinn et al. 2007). However, predictions of the interactive effects of
multiple anthropogenic factors on species based on their individual effects may
under or overestimate these effects because their interactive effect can be
complex (Dukes et al. 2011; Hoover et al. 2012). Experimental studies in
terrestrial (Hoover et al. 2012) and aquatic ecosystems (Doyle et al. 2005) have
shown that the interactive effect of multiple anthropogenic factors may be larger
(synergistic) or smaller (antagonistic) than their expected additive effects (Folt et
al. 1999; Darling and Côté 2008). Studies investigating interactive anthropogenic
factor effects on plant and consumer invasions are increasing, but our
understanding of these interactive effects on exotic plants and consumers at the
community level remains limited (Dukes and Mooney 1999; Vilà et al. 2007;
Didham et al. 2007; Tylianakis et al. 2008).
Warming can increase the survival, growth, and reproduction of exotic aquatic
plants (You et al. 2014) and aquatic animals (Sorte et al. 2010) by increasing the
length of the growing season and reducing winter mortality (Davis et al. 1998b;
91
Dukes and Mooney 1999; Rahel and Olden 2008; Walther et al. 2009). Studies
show that warming can enhance (Dukes and Mooney 1999; Sorte et al. 2010;
Chuine et al. 2012) or inhibit species invasions (Williams et al. 2007) and also
influence species interactions (Verlinden et al. 2014). For instance, warming
increased exotic Solidago gigantea dominance depending on the plant species
with which it was grown, suggesting that warming influences plant interactions
(Verlinden et al. 2014). Warming also increased exotic consumer herbivory
(Llorens et al. 2004; Rahel and Olden 2008), but herbivore effects on plants can
depend on warming effects on plants, suggesting that warming can alter plantherbivore interactions (van der Heide et al. 2006a). These studies show that our
understanding of the effects of warming on exotic plants, consumers, and
plant-herbivore interactions at the community level is limited.
Studies have investigated nutrient enrichment effects individually and in
combination with other anthropogenic environmental factors on terrestrial (Dukes
et al. 2011) and on aquatic plants (Wersal and Madsen 2011; You et al. 2014).
Elevated nutrients increase native and exotic plant growth, but frequently favor
exotic plants, increasing their dominance in invaded habitats (Daehler 2003;
Rickey and Anderson 2004; Scherer-Lorenzen et al. 2007; Tyler et al. 2007). The
dominance and performance of exotic plants often increases with available
resources because exotic plants often have characteristics that include rapid
growth rate and high phenotypic plasticity that allows them to quickly take
advantage of available resources, outcompeting native plants that do not
possess these characteristics (Kennedy et al. 2009). Similarly, elevated nutrients
92
may alter exotic consumer performance, but their effect on herbivores is not as
clear as for exotic plants because nutrient enrichment effects on exotic
consumers vary by species (Wikström and Hillebrand 2011). However, these
studies suggest that nutrient enrichment may increase plant and herbivore
invasions possibly altering native community structure (Kennedy et al. 2009).
Here we investigated the individual and interactive effects of warming and
nutrient enrichment on exotic plants and snails, on plant-herbivore interactions,
and their effect on native plants and snails in freshwater wetland communities
with a field mesocosm experiment. Specifically, we assessed the effects of 1)
elevated nutrients, increased temperature, and their interaction on native and
exotic snails and plants and 2) plant invasion effects on native plants and on
native and exotic snails in wetland communities.
5.4. Methods
5.4.1. Study system
The exotic aquatic plants Alternanthera philoxeroides (alligator weed Amaranthaceae), Eichhornia crassipes (water hyacinth-Pontederiaceae), Pistia
stratiotes (water lettuce-Araceae), and the exotic snail Pomacea maculata (island
apple snail–Ampullariidae; synonym P. insularum) (Hayes et al. 2012) are
sympatric in their native range (South America) and co-occur in heavily invaded
local wetlands in southeast Texas. These exotic species invade habitats
characterized by the native wetland plants Hydrocotyle umbellata (water
pennywort–Araliaceae), Limnobium spongia (frog's bit–Hydrocharitaceae),
93
Pontederia cordata (pickerelweed-Pontederiaceae), Typha latifolia (cattail Typhaceae), and the native snails Physella acuta (bladder snail- Physidae) and
Planorbella trivolvis (marsh ramshorn snail - Planorbidae) in the introduced
range. The plant species were selected in part based on their growth forms in
addition to being common. Native H. umbellata, P. cordata, T. latifolia and exotic
A. philoxeroides are emergent plants. In addition, H. umbellata and
A. philoxeroides can grow in both terrestrial and aquatic habitats. Exotic
P. stratiotes and E. crassipes and native L. spongia are free-floating aquatic
plants that reproduce clonally. Eichhornia crassipes and L. spongia have similar
phenotypes in varying environmental conditions. Moreover, native P. cordata and
E. crassipes are from the same family.
Alternanthera philoxeroides was introduced from the Parana River region of
South America (Julien et al. 1995). It was first recorded in Mobile, Alabama in
1897 and invaded coastal states from North Carolina to Texas by 1963 (Spencer
and Coulson 1976). In aquatic habitats, it anchors to banks and reproduces
clonally but does not produce viable seeds in the introduced range (Spencer and
Coulson 1976; He et al. 2014). Alternanthera philoxeroides has hollow stems that
root at the nodes, resulting in large interwoven mats or free-floating monocultures
when fragmented (Spencer and Coulson 1976; Sainty et al. 1997).
Eichhornia crassipes is considered one of the worst aquatic weeds in the
world with high socio-economic and ecological impacts (Lowe et al. 2004). It was
introduced from South America to the USA in 1884, invaded southern USA states
by the 1900’s, and its current exotic distribution includes more than 50 countries
94
on five continents (Lowe et al. 2004). This perennial herb is characterized by
free-floating rosettes with clonal reproduction; newly formed rosettes can break
easily, allowing them to disperse and colonize neighboring habitats.
Pistia stratiotes is on the list of the world’s worst weeds (Evans 2013). It was
introduced from South America to the United States where it was first reported in
Florida in 1765 (Stuckey and Les 1984). It is currently found in Europe, Africa,
and Asia (Neuenschwander et al. 2009). Pistia stratiotes may disperse and
colonize neighboring habitats by forming mats of free-floating rosettes that can
exist on their own or as interconnected clones.
Pomacea maculata’s native range extends north to the Amazon basin of
Brazil and also occurs in Uruguay and Paraguay (Karatayev et al. 2009). It was
discovered in 1989 in SE Texas with source populations likely from the lower
Parana River Basin in La Plata region of Argentina (Hayes et al. 2012). Pomacea
maculata populations have been reported along the Gulf Coast from Texas to
Florida and along the Atlantic coast to South Carolina (Rawlings et al. 2007;
Byers et al. 2013). These snails are voracious generalist plant consumers
(Rawlings et al. 2007) with high reproductive rates of an average of 2000 eggs
per clutch (Barnes et al. 2008). Pomacea maculata’s ecological impact on
wetland plant communities is similar to another apple snail P. canaliculata’s
impact on Asian wetlands (Carlsson et al. 2004) because it can significantly
reduce native plant survival, growth, and diversity by preferentially consuming
native plants than exotic plants in wetland communities (Meza-Lopez and
Siemann 2015).
95
5.4.2. Experimental setup
To investigate the individual and interactive effects of warming and nutrient
enrichment on exotic plants and snails, on plant-herbivore interactions, and the
effects on native plant and snail communities, we conducted a 2×2×2 factorial
field experiment that manipulated plant addition, nutrients, and temperature in
established freshwater wetland communities at Rice University South Campus
Field Station.
We established native wetland communities in fall 2011 by adding 15cm
topsoil/sand mixture and municipal water to 473L tanks. We then added an
individual of each native plant: L. spongia, H. umbellata, and P. cordata, and 40
of each native snail P. acuta and P. trivolvis to mesocosms. We added native
T. latifolia to all mesocosms and allowed it to establish for five months, while
other native plants got established for nine months. We replaced native plants
that did not survive after two weeks of the initial planting with a new individual to
ensure that all native species were represented in established plant communities.
In summer 2012, three juvenile P. maculata snails were introduced to
previously established native wetland plant communities randomly assigned to:
1) plant addition: native (L. spongia, H. umbellata, and P. cordata) or exotic
(A. philoxeroides, E. crassipes, and P. stratiotes), 2) nutrients: control (no
addition) or high (+6mg/L Nitrogen and +2mg/L Phosphorus), and 3)
temperature: ambient or +2°C with five replicates per treatment. We added a
total of 160g of plants that were either native (3 species) or exotic (3 species) to
each established native plant community to only manipulate plant origin (native
96
vs. exotic) in plant addition treatments. Nutrient treatments were based on
nutrient levels in southeast Texas waters. Nutrients were mixed with municipal
water before being added to wetland communities using a Dosatron and a flowthrough watering system that resulted in a four-day hydraulic residence time for
water in communities. In addition, we used four solar water heaters (each
1.2 x 6m, Specialty Pool Products, East Windsor CT, USA) to increase the water
temperature before delivering it to each community. For the duration of the study,
we conducted weekly P. maculata egg mass surveys and monthly visual plant
surveys. After 19 weeks, we harvested, sorted, dried, and weighed native and
exotic aboveground plant mass and collected and quantified native and exotic
snail abundance and size.
5.4.3. Data analyses
We used three-way ANOVAs to test the dependence of total, native, and native
plant species masses, native snail P. acuta and P. trivolvis abundances, and
exotic P. maculata size (operculum length) and mass on nutrients, temperature,
plant addition, and their interactions. We also tested the dependence of exotic
plant mass and exotic plant species’ masses on nutrients, temperature, and their
interaction with two-way ANOVAs. In addition, we conducted repeated measures
ANOVAs to test the dependence of P. maculata egg clutch number and egg
clutch mass on nutrients, temperature, plant addition, and their interactions. Data
met the assumptions of ANOVAs and repeated measures ANOVAs. Post-hoc
tests were performed to determine differences between treatment levels for
97
significant variables with more than two levels. We performed all statistical
analyses using SAS (v 9.4).
5.5. Results
5.5.1. Snails
Warming increased P. maculata egg clutch number with no effect of nutrients,
plant addition, or their interactions (Table 5-1). Pomacea maculata egg clutch
number changed over time and depended on the interaction of plant addition,
nutrients, and temperature over time (Table 5-1, “time”, “plant addition*nutrients*
temperature*time”, Appendix Figure 5-1a, Appendix Figure 5-4).
Pomacea maculata egg mass increased four-fold with warming while
nutrients, plant addition, and their interactions had no effect on egg mass (Table
5-1, Figure 5-2). Pomacea maculata egg mass changed over time and was
influenced by the interaction of plant addition, nutrients, and temperature over
time (Table 5-1, “time”, “plant addition*nutrients* temperature*time”, Appendix
Figure 5-1b).
Nutrients, temperature, and plant addition treatments did not affect
P. maculata mass (Table 5-1). However, elevated nutrients combined with
warming increased P. maculata mass (Table 5-1, “nutrients*temperature”, Figure
5-2 ). Other factor interactions did not affect P. maculata mass (Table 5-1,
Appendix Figure 5-2).
Elevated nutrients increased native P. acuta abundance with no effect of
temperature, plant addition, and their interactions (Table 5-1, Appendix
98
Figure 5-3). Nutrients, temperature, plant addition and their interactions had no
effect on native P. trivolvis abundance (all P > 0.05, Appendix Figure 5-3b).
5.5.2. Plants
Elevated nutrients increased total and native plant mass (Table 5-2). Warming
had no effect on total or native plant mass (Table 5-2). Nutrient and plant addition
interactions did not affect total plant mass (Table 5-2, “plant addition*nutrients”,
Figure 5-4a). Temperature together with plant addition treatments influenced total
and native plant mass (Table 5-2, “plant addition*temperature”, Figure 5-4b,d).
Other factor interactions did not affect total plant mass (Table 5-2, Appendix
Table 5-1). In addition, exotic plants on their own and in combination with
nutrients reduced native plant mass (Table 5-2, “plant addition*nutrients”,
Figure 5-4c). Additional factor interactions did not influenced native plant mass
(Table 5-2, Appendix Table 5-1).
Elevated nutrients increased native L. spongia, P. cordata, T. latifolia, and
H. umbellata mass (Appendix Table 5-2). Exotic plants reduced L. spongia,
P. cordata, and T. latifolia mass but had no effect on H. umbellata mass
(Appendix Table 5-2). Elevated nutrients and plant addition treatments increased
native plants L. spongia, P. cordata, and T. latifolia mass but had no effect on
H. umbellata (Appendix Table 5-2, Appendix Figure 5-4). Temperature and other
factor interactions did not affect native plant L. spongia, P. cordata, T. latifolia, or
H. umbellata mass (Appendix Table 5-1, Appendix Table 5-2).
Exotic plant mass increased with elevated nutrients while warming had no
effect on exotic plant mass (Table 5-2, Figure 5-3 e-f). Nutrients and warming
99
together had no effect on exotic plant mass (Table 5-2, Appendix Table 5-1,
“nutrients*temperature”). Elevated nutrients increased exotic plants E. crassipes
and A. philoxeroides mass while P. stratiotes was the most abundant exotic plant
in ambient nutrient treatments (Appendix Table 5-3, Appendix Figure 5-5).
Temperature and factor interactions had no effect on E. crassipes,
A. philoxeroides, or P. stratiotes mass (Appendix Table 5-1, Appendix Table 5-3).
5.6. Discussion
Warming increased exotic snail invasions with no nutrient enrichment effect, but
nutrient enrichment together with warming increased snail performance.
Warming increased P. maculata reproduction (egg clutch number and egg clutch
mass) and warming with elevated nutrients increased P. maculata adult mass,
suggesting that warming will increase P. maculata invasions. Elevated nutrients
increased native snail P. acuta abundance but had no effect on P. maculata. In
addition, warming had no effect on native snails. These results suggest that
nutrient enrichment and warming effects on snails may depend on the origin or
identity of snails. Similarly, warming effects on plants depended on plant origin
and plant identity. Warming reduced native plant mass and had no effect on
exotic plant mass, suggesting that warming may contribute to an increase in
exotic plant dominance. Furthermore, elevated nutrients increased total plant
mass but had greater effects on exotic plants compared to native plants,
suggesting that nutrient enrichment will increase the likelihood of plant invasions
and their dominance in invaded habitats. Together this suggests that warming
100
and nutrient enrichment may contribute to multiple plant and snail invasions in
these ecosystems.
Studies have shown that warming often increases invader success in
terrestrial (Dukes and Mooney 1999) and marine communities (Sorte et al. 2010;
Dijkstra et al. 2011). Warming may increase the likelihood of invader success by
altering an invader’s performance (growth and reproduction) and increasing the
length of the growing season (Cockrell and Sorte 2013) for invaders, specifically
invaders that originate from a warmer native range because warming would
make environmental conditions more similar to the conditions that invaders are
exposed to in their native range. For instance, warming increased the population
size of exotic tropical flies Drosophila simulans and D. melanogaster compared
to non-tropical D. obscura (Davis et al. 1998b). These results agree with our
findings and suggest that warming may increase exotic P. maculata reproduction
with an increase in temperatures by providing optimal conditions for reproduction.
Warming could also increase the length of the growing season in the introduced
range, resulting in an increase in P. maculata’s lifetime reproductive output but
we did not test this given the design and duration of our study.
Others have found that warming in combination with elevated nutrients
increased the performance of consumers similar to the observed increase in
P. maculata size in our study. For instance, warming and elevated nutrients
together increased native grassland herbivore abundance (de Sassi et al. 2012)
and native zooplankton density (O’Connor et al. 2009). De Sassi et al. (2012)
suggested that an increase in herbivore abundance may be a result of elevated
101
nutrient effects on exotic plants. Additional studies have shown that elevated
nutrient effects via changes in exotic plants increase the performance of exotic
grasshopper (Bownes et al. 2013a), a mirid bug (Coetzee et al. 2007), and a
weevil (Center and Dray 2010). In our study, elevated nutrients had greater
effects on exotic plants than native plants, suggesting that nutrient enrichment
can influence the performance of P. maculata. However, it is unlikely that
elevated nutrient effects via changes in exotic plants increased P. maculata size
because P. maculata has been shown to preferentially consume native plants
(Burlakova et al. 2009; Meza-Lopez and Siemann 2015). Even though
P. maculata can grow and survive when fed exotic plants (Burks et al. 2011),
their growth rate is higher when they consume lettuce compared to exotic plants
(Lach et al. 2000). These studies indicate that warming and elevated nutrients
increase exotic insect performance primarily via nutrient enrichment effects on
exotic plants but the mechanism by which warming and nutrient enrichment
influence P. maculata performance is unclear.
Elevated nutrients have been shown to increase the performance of
herbivores by increasing their growth (Rosemond et al. 1993; de Sassi et al.
2012). In our study, elevated nutrients had no effect on adult P. maculata snails
but increased native P. acuta snail abundance, suggesting that nutrient
enrichment may more strongly increase native snail population growth rates.
Similarly, phosphorus enriched water increased grazing caddisfly Leucotrichia
pictipes and Psychomyia flavida larval mass, developmental rates, and
population densities, and increased periphyton biomass. It was suggested that
102
an increase in the performance of aquatic herbivores with elevated nutrients
could be a result of increased periphyton quality and quantity with elevated
nutrients (Hart and Robinson 1990). In our study, elevated nutrients may have
increased P. acuta abundance by increasing periphyton mass, but our study did
not assess nutrient enrichment effects on periphyton performance. In addition,
our study was unlikely to detect nutrient enrichment effects on adult P. maculata
via periphyton because the diet of P. acuta and P. maculata vary depending on
their size. Physella acuta consumes periphyton (Wikström and Hillebrand 2011)
and adult P. maculata are voracious plant consumers (Rawlings et al. 2007).
However, P. maculata consumes periphyton as hatchlings and juveniles when
they are similar in size to juvenile and adult native snails and then switch from
periphyton to plants as they grow. These results suggest that nutrient enrichment
may increase the performance of native snails, but it is unlikely that it influences
P. maculata invasions via an increase in periphyton.
Warming had no effect on plant invasions but may reduce native plant mass.
It has been suggested that warming can reduce plant performance by increasing
heat or water stress (White et al. 2000). In our study, it is probable that warming
reduced native plant mass by increasing heat stress compared to water stress
because water levels in wetland communities remained constant throughout the
study. Furthermore, exotic plants reduced native plant mass, suggesting that
exotic plants may increase warming effects on native plants. This suggests that
warming in combination with plant invasions probably reduce native plant mass,
increasing plant invasion success.
103
Higher exotic plant mass than native plant mass with elevated nutrients,
suggests that elevated nutrients will magnify the effect of exotic plants on native
plants and increase exotic plant dominance. Elevated nutrients have been shown
to favor exotic plants and increase the dominance of exotic plants in terrestrial
(Huenneke et al. 1990; Brooks 2003; Mahdavi-Arab et al. 2014) and aquatic
ecosystems (Tyler et al. 2007; Gennaro and Piazzi 2014). In addition, nutrient
enrichment is known to increase exotic plant mass and competitive ability in
many ecosystems (Wedin and Tilman 1996; Brooks 2003; Tyler et al. 2007;
Mahdavi-Arab et al. 2014). In our study, E. crassipes had higher mass than
A. philoxeroides or P. stratiotes with elevated nutrients. In addition, P. stratiotes
only survived in low nutrient conditions, suggesting that nutrient enrichment can
also have negative effects on exotic aquatic plants depending on plant
interactions. Exotic plants may also outcompete other exotic plants in high
resource habitats. This may have been the case with P. stratiotes and
E. crassipes because E. crassipes can completely cover the surface of water
potentially crowding out native and other exotic plants. Furthermore, a model
predicted that elevated nutrients may increase exotic plant E. crassipes growth
ten-fold (Wilson et al. 2005). Exotic plants that have increased performance with
nutrient enrichment often have characteristics that include high growth rates and
high phenotypic plasticity that allows them to quickly take advantage of available
resources. However, native plant performance in some cases may be higher or
equivalent to exotic plants in habitats with low resource availability (Daehler
2003; Bradley et al. 2010). This suggests that environmental conditions can
104
significantly influence plant invasions and exotic plant impacts on native plants in
invaded ecosystems. In addition, P. maculata may enhance the effect of exotic
plants and nutrient enrichment on native plants because P. maculata
preferentially consumes native plants (Burlakova et al. 2009; Meza-Lopez and
Siemann 2015). However, we did not test P. maculata effects on native and
exotic plants because P. maculata was present in all native wetland communities
in our study. These results suggest that elevated nutrients will favor exotic plants
and nutrient enrichment in combination with exotic plants will further reduce
native plant performance, contributing to multiple plant invasions and an increase
in exotic plant dominance in nutrient enriched aquatic ecosystems.
Even though we did not detect significant positive or negative effects of
warming on exotic plants, warming may increase the likelihood of plant invasion
success because it reduces native plant performance. In addition, warming may
increase the performance of exotic plants in the introduced range by creating a
novel environment that closely resembles the environment in the exotic plant’s
native range especially for exotic species from warmer native ranges (Walther et
al. 2002). Warming may reduce winter frost events and increase the length of the
growing season, reducing annual winter exotic plant mortality and increase
growth and reproduction for species from warmer environments. For instance,
with warmer winters the exotic palm Trachycarpus fortune survived outdoors all
year without protection (Walther et al. 2007).Warming can also inhibit plant
invasions if it does not increase resource availability in invaded habitats, reducing
the probability that exotic plants become dominant and outcompete native plants
105
in invaded habitats (Bradley et al. 2010). These studies suggest that warming
may increase the likelihood of plant invasions when resources are available but
we did not observe this in our study.
In conclusion, our results indicate that warming alone and in combination with
nutrient enrichment will contribute to herbivore invasions and that nutrient
enrichment will increase the likelihood of plant invasion success, reducing native
plant mass in aquatic ecosystems. Furthermore, our results showed that the
interactive effects of multiple anthropogenic factors on native and exotic species
are complex and could not be predicted based on their individual effects. Effects
of anthropogenic factors alone and in combination varied depending on snail and
plant identity as well as their origin (native vs. exotic); therefore, additional
studies investigating the interactive effects of multiple anthropogenic factors on
multi-trophic invaders considering species interactions at the community level are
needed.
5.7. Acknowledgements
We thank: Steve Pennings for tanks; Chef Derrix at a Rice University Servery for
providing lettuce for snail populations; Hannah Chen, Cassandra Corrales,
Jordan Bunch, Dana Galvan, Josh Hwang, Hayden Ju, Daniel McDermott, Ariel
Nixon, Peter Sylvers, Candice Tiu, Ling Zhang, Qiang Yang, and Boris Zhong for
their assistance in the field and lab; Romi Burks, Jenn Rudgers, Amy Dunham,
Volker Rudolf, and Anna Armitage for helpful discussions. This work was
supported by a Ford Foundation Predoctoral Fellowship (to MML), an
106
Environmental Protection Agency Science to Achieve Results Fellowship for
Graduate Environmental Study (to MML), a Rice University Shell Center for
Sustainability research grant (to MML), and a Rice centennial award to support
undergraduate research (to MML).
107
Table 5-1 The dependence of exotic snail P. maculata egg clutch number, egg clutch mass, adult mass, and
native snail P. acuta abundance on nutrients, temperature, plant addition, and their interactions in ANOVAs or
repeated measures ANOVAs. Significant results are shown in bold
P. maculata
clutch #
P. maculata
egg mass
P. maculata
mass
P. acuta
abundance
Factor
DF
F
P
F
P
F
P
F
P
Nutrients
Temperature
Plant addition
Nutrients*temperature
Plant addition*nutrients
Plant addition*temperature
Plant addition*nutrients*temperature
Error
Time
Nutrients*time
Temperature*time
Plant addition*time
Nutrients*temperature*time
Plant addition *nutrients*time
Plant addition*temperature*time
Plant addition*nutrients*temperature*time
Repeated error
1
1
1
1
1
1
1
32
8
8
8
8
8
8
8
8
256
0.1
8.0
1.5
0.2
0.6
0.1
0.1
0.8193
0.0081
0.2354
0.6895
0.4595
0.8193
0.7319
0.5
9.9
1.0
0.8
0.9
0.1
0.0
0.4851
0.0036
0.3429
0.3785
0.3413
0.7228
0.9833
1.7
0.1
2.5
4.4
0.6
0.1
3.1
0.2036
0.8914
0.1254
0.0446
0.4434
0.9595
0.0868
8.5
0.2
0.1
1.9
0.1
0.3
0.3
0.0064
0.6429
0.9588
0.1813
0.7893
0.6164
0.6164
3.2
1.1
0.8
1.1
0.6
1.1
0.8
2.9
0.0018
0.3602
0.6496
0.3670
0.7539
0.3602
0.6496
0.0043
2.9
0.5
0.7
0.7
0.5
0.7
1.5
3.8
0.0043
0.8403
0.7256
0.6750
0.8756
0.6552
0.1424
0.0003
108
Table 5-2 The dependence of total, native, and exotic plant masses on nutrients, temperature, plant addition, and
their interactions in ANOVAs. Significant results are shown in bold
Total plant
mass
Native plant
mass
Factor
F1,32
P
F1,32
Nutrients
110.8
<0.0001
19.1
Temperature
1.0
0.3229
Nutrients*temperature
0.3
Plant addition
P
Exotic plant
mass
F1,16
P
0.0001
155.0
<0.0001
2.4
0.1345
0.5
0.5052
0.6118
0.4
0.5115
0.1
0.8845
0.8
0.3698
67.1
<0.0001
Nutrients*plant addition
0.3
0.5603
46.1
<0.0001
Temperature*plant addition
5.8
0.0222
5.3
0.0287
Nutrients*temperature*plant addition
0.1
0.7846
0.2
0.6934
109
(a) 8
(b)
Nutrients
Temperature
control
high
(c)
Plant addition
ambient
+2°C
native
exotic
Egg mass (g)
6
4
2
0
2
4
6
8
10
Time (week)
2
4
6
Time (week)
8
10
2
4
6
8
10
Time (week)
Figure 5-1 Exotic P. maculata snail egg clutch mass dependence on (a) nutrients, (b) temperature, and (c) plant
addition treatments over time. Means ±1SE
110
Pomacea maculata mass (g)
60
Nutrients
ab
45
control
high
ab
b
a
30
15
0
ambient
+2°C
Temperature
Figure 5-2 Exotic P. maculata snail mass dependence on nutrient and
temperature treatments. Means +1SE. Means with the same letters were not
significantly different in post-hoc tests
111
Physella acuta abundance
80
a
60
40
b
20
0
control
high
Nutrients
Figure 5-3 Native P. acuta snail abundance dependence on nutrient
treatments. Means +1SE. Means with the same letters were not significantly
different in post-hoc tests
112
Total plant mass (kg)
(a) 4
Nutrients
(b)
control
high
3
Temperature
ambient
+2°C
a
ab
a
b
2
1
0
Native plant mass (kg)
(c) 4
(d)
Nutrients
a
3
Temperature
ambient
+2°C
control
high
a
b
2
b
bc
1
c
c
c
0
Exotic plant mass (kg)
(e) 4
3
(f)
Nutrients
control
high
a
Temperature
ambient
+2°C
2
1
b
0
native
exotic
Plant addition
native
exotic
Plant addition
Figure 5-4 (a) Total plant mass dependence on nutrients together with plant
addition and (b) on temperature together with plant addition treatments. (c)
Native plant mass dependence on nutrients together with plant addition
and (d) on temperature together with plant addition treatments. (e) Exotic
plant mass dependence on nutrients and (f) on temperature. Means +1SE.
Means with the same letters were not significantly different in post-hoc
tests
113
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126
P. maculata shell length (mm)
25
a
b
a
20
a
15
c
b
10
b
b
E. c.
A. p.
5
0
Control
Low
High
Nutrients
Lettuce
Plants
Appendix Figure 3-1 The dependence of P. maculata snail shell length on
(a) nutrients and (b) plants in experiment 1. Means +1SE. Means with the
same letters were not significantly different in post-hoc tests.
E. c. = E. crassipes, A. p. = A. philoxeroides
127
Wet plant mass (g)
a
L. spongia
b
H. umbellata
45
30
a
15
b
0
Wet plant mass(g)
c
a
E. crassipes
d
A. philoxeroides
45
b
a
30
b
15
0
No snails
Snails
Snails
No snails
Snails
Snails
Appendix Figure 3-2 The dependence of (a) L. spongia, (b) H. umbellata, (c)
E. crassipes, and (d) A. philoxeroides wet plant mass on snails in
experiment 2. Means +1SE. Means with the same letters were not
significantly different in post-hoc tests
128
5
0.0
-0.4
0
1
-1
0
-0.8
0.0
-0.4
-0.8
-1.2
0
1
-1
Axis 1
-0.4
1
0.0
-0.4
0.0
-0.4
1
2
0
0.4
1
0.0
-0.4
2
0.4
0.0
1
2
j. native + exotic
L. spongia ( =0.8kg)
0.8
0.4
0.0
-0.4
-1.2
-1
0
1
2
Axis 1
-0.4
0
-0.8
-2
m. native only
T. latifolia
( =1.5kg)
0.8
-1
Axis 1
-1.2
-1
-2
i. native only
L. spongia
( =0.8kg)
Axis 1
Axis 2
0.4
0
-0.8
-2
2
l. native + exotic
H. umbellata
( =0.3kg)
0.8
Axis 2
0.4
0.0
Axis 1
k. native only
H. umbellata
( =0.3kg)
0.8
0
-1.2
-1
0.8
-1.2
-2
2
0.4
-0.4
Axis 1
h. native + exotic
P. cordata
( =0.1kg)
0.8
0.0
-0.8
-2
1
0.4
-2
-1
0
1
2
Axis 1
n. native + exotic
T. latifolia
( =1.5kg)
0.8
Axis 2
-1
0
-0.8
-1.2
-2
-0.4
Axis 1
Axis 2
0.4
0.4
-1.2
-1
2
g. native only
P. cordata
( =0.1kg)
0.8
Axis 2
Axis 2
0.0
-0.4
Axis 2
1
0.0
e. exotic only
P. stratiotes
( =0.1kg)
0.8
-0.8
Axis 2
f. native + exotic
P. stratiotes
( =0.1kg)
0.4
10
Axis 1
Axis 1
0.8
0.4
15
0
-1.2
-1
d. native + exotic
A. philoxeroides
( =0.4kg)
0.8
5
-0.8
0
c. exotic only
A. philoxeroides
( =0.4kg)
Axis 2
10
20
Axis 2
0.4
15
25
b. native + exotic
E. crassipes
( =1kg)
0.8
Axis 2
a. exotic only
E. crassipes
( =1kg)
Axis 2
Rank
20
Rank
25
0.0
Temp - nutrients
+0C - control
+1C - control
+2C - control
+0C - high
-0.4
+1C - high
-0.8
-0.8
-0.8
-0.8
-1.2
-1.2
-1.2
-1.2
-2
-1
0
Axis 1
1
2
-2
-1
0
Axis 1
1
2
-2
-1
0
Axis 1
1
2
+2C - high
-2
-1
0
1
2
Axis 1
Appendix Figure 4-1 The dependence of exotic (a-b) E. crassipes, (c-d) A. philoxeroides, and (e-f) P. stratiotes
and native (g-h) P. cordata, (i-j) L. spongia, (k-l) H. umbellata, and (m-n) T. latifolia in relation to nutrients and
temperature in exotic or native only communities and communities with both native and exotic plants. Symbol
size represent species dry plant mass
129
Nutrients
control
high
a
1.2
0.8
0.4
b
0.0
(b) 2.0
a
E. crassipes mass (kg)
L. spongia mass (kg)
(a) 1.6
1.6
1.2
b
0.8
0.4
b
b
0.0
native
Nutrients
control
high
c
d
native + exotic
Community composition
exotic
native + exotic
Community composition
Appendix Figure 4-2 (a) Native L. spongia and (b) exotic E. crassipes mass
dependence on community composition and nutrients. Bars represent
+1SE. Means with the same letters were not significantly different in
post-hoc tests. Scale is different for each species
130
a temperature*nutrients*plant addition
+2°C, control, native
+2°C, high, native
+2°C, control, exotic
+2°C, high, exotic
2.0
16
ambient, control, exotic
ambient, high, exotic
ambient, control, native
ambient, high, native
Egg mass (g)
Egg clutch number
2.5
1.5
1.0
temperature*nutrients*plant addition
b
+2°C, control, native
+2°C, high, native
+2°C, control, exotic
+2°C, high, exotic
ambient, control, exotic
ambient, high, exotic
ambient, control, native
ambient, high, native
12
8
4
0.5
0.0
0
2
4
6
Time (week)
8
10
2
4
6
8
Time (week)
Appendix Figure 5-1 Exotic P. maculata snail (a) egg clutch number and (b) egg mass dependence on the
interactive effect of temperature, nutrients, and plant addition treatments over time. Means ± 1SE
10
131
60
P. maculata mass (g)
50
Plant addition
native
exotic
40
30
20
10
0
control, ambient
control, +2°C
high, ambient
high, +2°C
Nutrient - temperature treatments
Appendix Figure 5-2 Pomacea maculata snail mass dependence on plant
addition, nutrients, and temperature treatments. Means +1SE
132
a
120
Plant addition
native
exotic
b
100
80
P. trivolvis abundance
P. acuta abundance
100
60
40
20
Plant addition
native
exotic
80
60
40
20
0
am
,
l
ro
nt
o
c
nt
bie
l,
tro
n
co
°C
+2
m
,a
h
g
bi
0
t
en
hi
h,
hig
°C
+2
Nutrient - temperature treatments
l,
ro
t
n
co
am
bie
nt
nt
l
tro
n
co
C
2°
+
,
hi
m
,a
h
g
bie
C
2°
+
h,
g
i
h
Nutrient - temperature treatments
Appendix Figure 5-3 (a) P. acuta and (b) P. trivolvis snail dependence on plant addition, nutrients, and
temperature treatments. Means +1SE
133
(a) 0.16
(b) 2.4
Nutrients
Plant mass (kg)
Nutrients
control
high
0.12
1.8
L. spongia
H. umbellata
0.08
control
high
a
1.2
b
bc
0.04
0.6
c
0.00
0.0
(c) 0.4
b
Nutrients
(d) 0.9
Nutrients
control
high
Plant mass (kg)
control
high
a
0.3
P. cordata
T. latifolia
0.6
0.2
0.3
a
b
b
b
a
0.1
a
0.0
0.0
native
exotic
Plant addition
native
exotic
Plant addition
Appendix Figure 5-4 Native (a) H. umbellata (no significant interactive
result), (b) L. spongia, (c) P. cordata, and (d) T. latifolia mass dependence
on nutrients and plant addition treatments. Means +1SE. Means with the
same letters were not significantly different in post-hoc tests. Note that the
y-axis scales differ among species
134
(a)
2.5
a
E. crassipes
(b) 0.6
(c)
A. philoxeroides
Plant mass (kg)
a
0.009
P. stratiotes
a
2.0
0.4
0.006
1.5
1.0
0.5
0.2
b
0.003
b
0.0
control
high
Nutrients
b
0.000
0.0
control
high
Nutrients
control
high
Nutrients
Appendix Figure 5-5 Exotic (a) E. crassipes, (b) A. philoxeroides, and (c) P. stratiotes mass dependence on
nutrient treatments. Means +1SE. Means with the same letters were not significantly different in post-hoc tests.
Note that the y-axis scales differ among species
135
Appendix Table 3-1 The dependence of native L. spongia and H. umbellata and exotic A. philoxeroides and
E. crassipes wet plant mass in experiment 2 on nutrients, snails, and their interactions in ANOVAs. Significant
results are shown in bold
L. spongia
Factor
Nutrients
Snails
Nutrients*snails
df
Fx,18
2
1
2
3.0
2.5
1.1
P
0.0744
0.1350
0.3623
H. umbellata
Fx,18
1.8
4.7
1.2
P
0.1931
0.0431
0.3228
A.
philoxeroides
Fx,18
P
1.0
55.2
2.5
0.3963
<0.0001
0.1110
E. crassipes
Fx,18
0.3
8.3
0.8
P
0.7316
0.0099
0.4658
136
Appendix Table 4-1 The dependence of percent cover on community
composition, nutrients, temperature, and their interaction in repeated
measures ANOVAs. Significant results are shown in bold
Factor
DF
Composition
1
Nutrients
Temperature
1
2
Composition*nutrients
Composition*temperature
Nutrients*temperature
Composition*nutrients*temperature
Error
Time
Composition*time
Nutrients*time
Temperature*time
Composition*nutrients*time
Composition*temperature*time
Nutrients*temperature*time
Composition*nutrients*temperature*time
Repeated error
1
2
2
2
36
7
7
7
14
7
14
14
14
252
Native plant
% cover
Exotic plant
% cover
F
P
F
27.4
51.0
1.5
<0.0001
<0.0001
0.2346
39.6
1.2
1.0
0.9
<0.0001
0.3223
0.3632
0.3994
52.2
16.7
20.0
1.1
<0.0001
<0.0001
<0.0001
0.3447
20.8
1.4
1.7
1.5
<0.0001
0.1812
0.0630
0.1092
P
2.8
0.1041
286.5
0.1
1.4
0.6
0.1
0.5
<0.0001
0.8884
0.2475
0.5719
0.9023
0.6114
35.8
1.4
<0.0001
0.2092
56.0
1.7
0.9
1.2
1.7
1.2
<0.0001
0.0604
0.5383
0.3027
0.0680
0.2793
137
Appendix Table 4-2 The dependence of exotic plant masses on nutrients,
temperature, and their interaction in ANOVAs. Significant results are
shown in bold
Factors
Nutrients
Temperature
Nutrients*temperature
A. philoxeroides E. crassipes
mass
mass
DF Fx,16
P
F x,16
P
1
1
1
55.4
2.8
2.5
<0.0001
0.1113
0.1340
72.6 <0.0001
0.9
0.3561
0.3
0.6256
P. stratiotes
mass
F x,16
P
19.1 0.0005
0.6 0.4468
0.6 0.4468
138
Appendix Table 5-1 Total and native plant mass and individual native species mass dependence on plant
addition, nutrients, and temperature. Exotic plant mass and individual exotic species mass dependence on
nutrients and temperature. Means±SE
Treatment
Exotic, control,
ambient
Exotic, control,
+2°C
Exotic, high,
ambient
Exotic, high,
+2°C
Native, control,
ambient
Native, control,
+2°C
Native, high,
ambient
Native, high,
+2°C
Total plant
Native plant
Exotic plant
H.
umbellata
P.
cordata
T.
latifolia
948.5±264
719.3±268
229.3±040
22.3±14
67.1±15
170.5±052
1338.8±377
1008.0±255
330.7±122
37.0±22
41.1±07
3071.8±282
504.9±116
2567.0±308
56.3±21
3180.9±220
456.3±120
2724.5±181
1369.2±377
L.
spongia
P.
stratiotes
A.
philoxeroides
E.
crassipes
459.4±260
5.9±2
53.2±05
170.1±038
290.7±057
639.2±187
8.5±2
47.4±05
274.8±126
60.8±16
113.7±068
274.2±080
0
542.5±67
2024.5±370
29.5±21
78.7±58
233.1±080
115.1±069
0
365.5±84
2359.1±243
1369.1±377
28.3±15
89.5±18
251.5±121
999.8±289
803.6±083
803.6±083
15.1±09
109.0±29
140.7±036
538.8±107
3184.2±127
3184.2±127
146.6±44
349.7±45
749.3±160
1938.5±248
2534.1±270
2534.1±270
62.9±37
299.2±62
575.1±154
1596.9±159
139
Appendix Table 5-2 The dependence of native plant masses on nutrients, temperature, plant addition, and their
interactions in ANOVAs. Significant results are shown in bold
Factors
H. umbellata
L. spongia
mass
mass
DF Fx,32
P
F x,32
P
Nutrients
1
6.8
0.0136
5.6
0.0243
Temperature
1
2.2
0.1488
2.1
0.1607
Plant addition
1
2.1
0.1535
Nutrients*temperature
1
2.3
0.1379
Plant addition*nutrients
1
3.6
0.0670
Plant addition*temperature
1
1.3
0.2581
2.3
Plant addition*nutrients*temperature
1
0.2
0.6950
0.7
43.4 <0.0001
0.2
P. cordata
mass
F x,32
P
20.7 <0.0001
0.1
T. latifolia
mass
F x,32
P
8.1 0.0078
0.7142
0.1 0.8756
32.1 <0.0001
10.0 0.0035
0.6897
0.1
0.8062
0.1 0.8252
24.7 <0.0001
15.7
0.0004
13.2 0.0010
0.1403
0.1
0.8298
3.3 0.0779
0.4062
1.2
0.2896
0.1 0.8298
140
Appendix Table 5-3 The dependence of exotic plant masses on nutrients,
temperature, and their interaction in ANOVAs. Significant results are
shown in bold
Factors
Nutrients
Temperature
Nutrients*temperature
DF
1
1
1
A. philoxeroides
mass
Fx,16
P
55.4
2.8
2.5
<0.0001
0.1113
0.1340
E. crassipes
mass
F x,16
P
72.6
0.9
0.3
<0.0001
0.3561
0.6256
P. stratiotes
mass
F x,16
P
19.1
0.6
0.6
0.0005
0.4468
0.4468
141