Growth, regeneration and colonisation of Egeria ...

Partie 2 | Chapitre 3

Impact de l’augmentation de températures automnales sur Egeria densa

Growth, regeneration and colonisation of Egeria densa fragments: the effect of autumn temperature increases G. Thiébauta, M. Gillarda, C. Deleub a UMR CNRS ECOBIO 6553, University of Rennes 1, 263 avenue Général Leclerc, 35042 Rennes, France b UMR 1349 INRA-Agrocampus Ouest-Université Rennes 1 IGEPP, University of Rennes 1, 263 avenue du Général Leclerc, 35042 Rennes, France

Aquatic Ecology (2016) 50(2), 175-185 DOI 10.1007/s10452-016-9566-3 Abstract The present study analysed the influence of higher temperatures on the growth, regeneration and colonisation abilities of apical shoot fragments from three naturalised and one cultivated population of Egeria densa. Our hypotheses were that (1) increased temperatures would favour the growth, regeneration and colonisation of E. densa shoots and (2) fragments from naturalised populations would have higher establishment success than fragments from cultivated plants. We tested the effect of average minimal autumn temperature (9°C), average maximal autumn temperature (16°C) and an increase of 3°C above these values, on apical shoots of these four populations of E. densa under controlled conditions in two growth chambers. Our results showed that temperature and the origin of the population had an effect on the growth rate of E. densa fragments, on their regeneration and colonisation abilities at the maximal autumn temperature. An increase of 3°C stimulated the growth rate of E. densa at low temperatures but had no effect on the plant colonisation and regeneration abilities. The responses of populations to low temperatures (9-12°C) were more similar than expected. In contrast, at higher temperatures (1619°C) the cultivated population showed lower apical growth, higher regeneration and similar colonisation abilities to the naturalised populations. At these higher temperatures, the responses also differed among the naturalised populations. These results suggest that global warming has implications for the invasiveness of E. densa. Keywords: Invasive macrophytes · Global warming · Establishment success · Functional traits 1. Chapitre 3 2. Chapitre 3 3. Chapitre 3

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Impact de l’augmentation de températures automnales sur Egeria densa

3.1. Introduction

other factors, on their thermal acclimation.

Climate change, variability and changes in

Phenotypic plasticity and rapid evolution

land use are major drivers of ecosystem

allow some invasive species to be more

alterations. Non Indigenous Species (NIS)

responsive to warmer autumn temperatures

also contribute to ecosystem changes. They

and to later freezing events than many native

cause

damage, and have

species (Richards et al. 2006), but there is a gap

economic consequences and impacts on

in our knowledge regarding invasive aquatic

human-health. Interactions exist between

plant establishment and its responses to

these threats and they could exacerbate the

predicted climate change.

environmental

Among the invasive macrophyte species,

impacts of climate change on ecosystems by and

Egeria densa Planch (Hydrocharitaceae), has

climate change may also enable further

been introduced worldwide by aquarium trade.

invasions (Hellmann et al. 2008; Mainka and

Hence, E. densa has been included in the

Howard 2010). Climate change could also

database of global invasive species (GISD

affect the dynamics of plant invasions by

2015), by the Invasive Species Specialist

favouring individual traits of invasive species

Group (ISSG) of the Species Survival

(Hellmann

Commission of the International Union for

changing

environmental

et

al.

2008).

conditions,

Aquatic

non-

indigenous plants could benefit from the

Conservation

of

Nature

(IUCN)-World

increasing seasonality and more marked wet

Conservation Union, although it is not in their

and dry cycles.

top 100 list (Curt et al., 2010). E. densa is a

In addition to physical changes, climate

perennial dioecious aquatic plant native from

change can alter ecosystems and species’ life

South America, in the neotropical range

cycles (Fitter et al. 1995; Bradley et al. 1999).

(Yarrow et al. 2009). In its introduced range, in

Scientists have traditionally focused their

Europe and in the United States, only male

attention on the seasonal changes in spring

flowers have been observed, thus plants

rather than those later in the year. Many

reproduce asexually by fragmentation (Cook

studies have focused on spring events in

and Urmi-König 1984). The large stands often

temperate regions, while studies on the basic

seen in the US, Canada, New Zealand, Japan

triggers of autumnal plant changes are, by

and Europe are considered to be genetic

comparison, in their infancy. Gallinat et al.

monocultures in each of these countries

(2015) consider that it is important to

because of this sole reproduction strategy

investigate the role of autumn climate change

(Kadono et al. 1997; Darrin 2009). E. densa

on NIS. The survival of invasive aquatic

was introduced to France in the 1920s as

macrophytes in ecosystems depends, amongst

experimental botanical material (St John

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Impact de l’augmentation de températures automnales sur Egeria densa

1961). These plants were released into the

new

wild and have become naturalised in France,

regeneration (the ability of fragments to grow

where their distribution has spread (Feuillade

new shoots and rhizomes), and establishment

1961a; 1961b). E. densa is found in both lentic

(the ability of fragments to develop roots and

and lotic environments (Yarrow et al. 2009)

become attached to the sediment) (Barrat-

and it appears to be confined to warm-

Segretain et al., 1998; Riis et al., 2009).

temperate and cool subtropical conditions.

Although abiotic variables may also influence

Within subtropical and tropical areas, E. densa

the survival and colonisation success of plant

is limited to high altitudes or cold-water

fragments,

springs (Cook and Urmi-König 1984). It is

propagules are little known. In the Upper

well adapted to cold climates and can survive

Parana River basin, physical and chemical

freezing conditions during the winter by

properties of the water seem to be related to

storing starch in its leaves and stems. It then

sediment characteristics, and plant fragments

uses

once

reaching habitats with different physical and

temperatures rise above 10°C. It can even live

chemical properties may differ in their

for a while under ice (Cook and Urmi-König

colonisation and growth success (Silveira et al.,

1984). The optimum growth temperature

2009). The spread of E. densa is a range

reported

maximum

expansion from established populations via

temperature for growth is 25°C (Cook &

dispersal by water or via unintentional

Urmi-König, 1984). Its growth is affected by

introduction by humans (emptying aquariums,

temperature (Barko and Smart 1981; Riis et al.

propagation of fragments attached to boats,

2012; Hussner et al. 2014) but not by CO2

etc.). The present study analysed the influence

availability under experimental conditions

of increasing autumn temperatures on the

(Hussner et al. 2014). E. densa biomass has two

growth, regeneration and colonisation abilities

growth maxima in August and December-

of E. densa shoots from different populations

January in Japan (Haramoto and Ikusima

during the first stage of the introduction

1988) and in late summer and late autumn in

process. We tested four populations: three

South Carolina (Getsinger and Dillon 1984).

“naturalised”

these

is

supplies

16°C

for

and

growth

the

site

by

plant

their

fragments

effects

on

populations

requires

vegetative

and

one

During the introduction phase, non-native

“cultivated” population (from an aquarium

aquatic species are usually introduced as stem

supply store). Our hypotheses were that (1) an

fragments. Vegetative propagules such as stem

increase of three degrees would favour

fragments, are essential for the dispersal and

growth, regeneration and colonisation of E.

colonisation of Hydrocharitaceae species

densa

(Silveira et al., 2009). The colonisation of a

70

fragments

and

(2)

naturalised

Partie 2 | Chapitre 3

Impact de l’augmentation de températures automnales sur Egeria densa

populations would have higher establishment

Two experiments were carried out in

success than a cultivated population.

autumn 2013. Climate change predictions for northern

3.2. Methods

latitudes

suggest

an

average

temperature increase of around 3°C over the

3.2.1. Experimental design

course of this century (McKee et al. 2003). To

Three sites A (N47°44'44''; W02°15'05''), B

keep our experiment in line with these

(N47°41'20''; W01°55'37'') and C (N47°37'39'';

predictions, we subjected the plants from the

W01°51'35'') characterised by the presence of

four populations to two experiments with a

dense monospecific beds of E. densa were

temperature increase of 3°C. Experiment 1

selected in Brittany, France. To characterise

consisted of testing the average minimal

the environmental conditions in which E.

autumn temperature (9°C) and a temperature

densa was growing, we assessed the water

3°C above this value, i.e. 12°C. In experiment

quality of each site over the course of one

2, we tested the average maximal autumn

year. At each sampling site, a water sample

temperature (16°C), and warmer conditions of

was collected in May, June, July, October and

19°C.

November 2013. Water temperature and the percentage

oxygen

were

controlled conditions in two growth chambers

whereas

other

(Percival AR-41L3X and Percival AR-41L3X

parameters such as pH, conductivity and

LT). Water temperatures were maintained at

measured

of in

dissolved

Each experiment was set up under

the

34

field, + 4

3

nutrients (PO , NH , NO ) were analysed in

specified levels (±1°C) using a temperature

the laboratory. Conductivity and pH were

regulated chamber possessing both heating

measured using a combined glass electrode

and cooling capacities. At the beginning of the

and

(25°C).

experiment, the shoots from each population

Reactive soluble phosphorus, nitrates and

of E. densa were cleaned gently by hand to

ammonia

a

remove invertebrates, algae and debris. To

standard

each transparent plastic container (with

molybdenum blue analytical technique for

dimensions L x W x H: 8 cm x 8 cm x 20 cm),

phosphates and by the indophenol technique

we added sediment composed of 1 cm of

for ammonia, AFNOR, 1990).

substrate (potting soil) overlaid with 1cm of

corrected

for

were

spectrophotometer

temperature analysed (by

the

using

In autumn 2013, forty shoots of E. densa

sand. Containers were filled with 500ml of tap

were collected from each site (populations A,

water ([NH4+–N] = 0.030 mg/l; [NO3-–N] =

B and C) and forty shoots of E. densa were

5.77 mg/l; [PO43-–P] = 0.010 mg/l; pH =

collected from a grower in the aquarium trade

8.17; conductivity: 486 µS/cm). A 10 cm-long

(population D). Shoots of population D had

apical shoot (with green leaves and without

been grown at 26°C in the store. 71

Partie 2 | Chapitre 3

Impact de l’augmentation de températures automnales sur Egeria densa

roots, lateral shoots or flowers) was put into

developed from nodes of the original apical

each plastic container. There were 10

shoot and other lateral shoots that developed

replicates

and

either from the same nodes, or from nodes of

experimental temperature. The fragments

the lateral shoots (Di Nino et al., 2007). We

grew under 330 µmol photons m-² s-1 as E.

also measured the length of lateral shoots

densa is reported to have optimum growth

(mean value), the mean root length and the

under these light conditions (Riis et al. 2012) in

area of a leaf located below the three-cm long

a 12/12 h light/dark cycle. The containers had

apex. The difference between the stem length

randomly assigned positions in the growth

at the beginning and the end of the

chambers.

experiment indicated the relative growth rate

for

each

population

The impact of increasing temperatures on

“RGR” (Silveira et al., 2009).

the growth of the fragments of E. densa was

RGR =

examined at the four temperature levels (9°C

L1 and L2 refer to total length at times 1 and

and 12°C, 16°C and 19°C) after 10 days of exposure,

when

the

experiments

(ln L2 − ln L1) (t2 − t1)

2.

were

3.2.2. Statistical analyses

concluded. Pistori et al. (2004) showed that the Relative Growth Rate of E. densa was the

The normal distribution of the values and

highest between 8 to 12 days after the

homogeneity of variance were checked, and a

beginning of an experiment.

two–way ANOVA was performed to test the

We measured 9 morphological traits at the

temperature and the population effects in

end of the experiment: stem length (distance

experiments 1 and 2. For each significant

from shoot base to the shoot apex), internode

difference (p