The Society Islands (French Polynesia) include fourteen tropical islands stretching between 16°29'40" – 17°52'30"S and 148°04'21" – 151°44'26"W for a total land area of 1,593 km² among which the high volcanic island of Tahiti occupies 1,045 km² (66%; Dupon et al. 1993). The geology of the volcanic island of Tahiti is dominated by basaltic lavas with a geological age ranging from 300,000 years on the Peninsula of Tahiti Iti to one million years on the larger volcano of Tahiti Nui (Brousse et al. 1985). The climate of Tahiti is characterized by the persistence of trade winds, an average annual temperature of 26 °C and the existence of two seasons: a dry season (May to October) with lower rainfall and temperatures (20 to 22 °C), and a rainy season (November to April) dominated by higher precipitation and temperatures (28 to 29 °C) (Laurence et al. 2004). Tahiti has a leeward dry west coast and a windward wetter east side exposed to the dominant southeastern trade winds. Thus, rainfall ranges from 1,000 mm year^-1 at sea level on the leeward coast to more than 5,000 mm year^-1 on the windward coast. Tahiti has three summits above 2,000 m, the highest peak reaching 2,241 m (Mt Orohena). Different plant formations are found according to elevation and rainfall: coastal vegetation near sea-level, mesic to moist forests (< 3,000 mm/year) at low- to mid-elevation and on exposed ridges, moist to wet forests (> 3,000 mm/year) at low- to mid-elevation, montane cloud forest starting at ca. 900 m on the leeward coast and 300–400 m on the windward coast, and subalpine shrubland found above 1,800 m (Papy 1954, Florence 1993, Meyer and Salvat 2009, Meyer 2010).

Spathodea is a large evergreen tropical tree reaching more than 30 m in height (Unwin 1920) with a trunk diameter of 0.50–1.75 m and a dense crown (Holdridge 1942, Little and Skolmen 1989). Spathodea originated from lowlands of Equatorial region, from west coast of Africa to central Africa between 12°N and 12°S (Irvine 1961), in areas with a wet and warm equatorial climate characterized by abundant rainfall and a monthly mean temperature above 26 °C (Francis 1990). Spathodea can be found on acid or basic soils, from loamy sands to clayey soils, with excessive to poor soil drainage and can survive in areas with a dry season of one to three months (Eliovson 1962). Successful reproduction has been reported at a minimum of 1,300 mm year^-1 (Francis 1990).

Spathodea produces numerous red-orange flowers pollinated by birds and bats in its native range (Keay 1957) but requires cross-pollination (Bittencourt et al. 2003). It reproduces mainly by seeds but can also reproduce via suckers from roots or branches (Little and Skolmen 1989). The wind-dispersed seeds are contained in a brown pod, each pod containing about 500 seeds (Little and Skolmen 1989, Fosberg et al. 1993) able to breach the ‘barrier effect’ of the trees present in forest edges (Staples et al. 2000, Labrada and Díaz Medina 2009). Spathodea has been listed as one of the world’s worst invasive alien species (Invasive Species Specialist Group 2004) and is considered as a major threat to native biodiversity in many Pacific islands (Pacific Islands Ecosystems at Risk 2011).

We counted the number of Spathodea (abundance) along a 6.2 km long elevational transect located on the leeward coast of Tahiti Nui from 140 to 1,300 m (between Belvédère road and Mt Aorai trail, lower end of the transect: 17°32'54"S-149°32'35"W, upper end of the transect: 17°32'5"S-149°30'30"W) (Figure 1). The number of Spathodea plants (≥ 3 m in height) was counted in plots from observation points on both sides of the elevational transect in a corridor ca. 20 m wide. Each counting point observation (n = 124 plots) included an area ca. 200 m² (~20 m x 5 m on left and right sides of the elevational transect) with a mean distance ca. 50 m between each point. These 124 points were geo-referenced with a handheld Global Positioning System (GPS Trimble® GeoXH^TM). Along the elevational transect, slope steepness was assessed with a 5 m-resolution Digital Elevation Model (DEM) of Tahiti processed in a Geographic Information System (GIS Mapinfo® Professional version 10, WGS 1984 projection).

Figure 1.

Study site with location of the area invaded by Spathodea campanulata on Tahiti Nui and Tahiti Iti (dashed black line) with the 6.2 km long elevational transect on Tahiti Nui (thick black line) and plant locations used for photosynthesis measurements (white circles).

The micro-climate was characterized at different elevation ranges by using temperature (°C), atmospheric humidity (%), and dew-point temperature (°C) recorded by iButtons (Hygrochron DS 1923). Dew-point temperature has been used to estimate the presence of extra precipitation from fog at different elevations. For example, on the island of Maui (Hawaiian Islands) fog may add important amounts of precipitation between the lifting condensation level at ca. 1,000 m elevation and the upper cloud limit set by the tradewind inversion at ca. 1900 m (Juvik and Ekern 1978, Kitayama and Muller-Dombois 1994, Loope and Giambelluca 1998).

Among the 124 plots surveyed, 10 iButtons were placed in ten plots along the elevational transect from 140 to 1,300 m. The number of Spathodea ranged from 0 to 18 in plots fitted with iButtons. They were programmed to record data every two hours (12 recordings per day) and then set on a tree trunk at 2 m above the ground. IButtons were exposed to the north in the understory. Measurements were recorded during 84 days from July to October, i.e. during the coldest and driest season in French Polynesia. Stress experienced during the dry season could limit survival or growth of Spathodea, thus we expect that a record of micro-climate during this critical period may provide useful information about environmental tolerances of Spathodea at mid-high elevation.

We measured in situ some aspects of leaf-level photosynthesis of Spathodea using a Pulse Amplitude Modulation fluorometer (PAM, Walz GmbH Chlorophyll-Fluorometer). PAM is a rapid, non-invasive tool to investigate physiological indicators of photosynthetic rate or stress (Bité et al. 2007, Guidi and Calatayud 2014). In this study, we measured leaf chlorophyll (Chl) fluorescence parameters for plants exposed to ambient light conditions. We used the following light curve-derived parameters:

1. Chl fluorescence Fo’ is the minimal fluorescence yield of illuminated sample with all photosystem PS II centers open (Guidi and Calatayud 2014). Chl fluorescence Fo’ is inversely correlated to photosynthetic efficiency (Bité et al. 2007), thus providing information about plant health (e.g. Percival 2005, Nikolić et al. 2008);

2. Maximum electron transport rate (ETR_max) reflects maximum flow of electrons, a measure of how quickly electrons can move through the photosystem (Bité et al. 2007). It is related to maximum photosynthetic rate (Edwards and Baker 1993, Eichelman et al. 2004);

3. Effective quantum yield Y(II) [Y(II)effective = (Fm’-F’)/Fm’], where Fm’ is the maximum Chl fluorescence yield in light conditions recorded immediately after a saturating pulse of light and F’ is the value where Chl fluorescence reaches a steady-state level, a measure of the photochemical conversion in light exposed leaves (i.e. the photosynthetic efficiency of photosystem II) (Guidi and Calatayud 2014). It assesses how efficiently the light is being used in photochemistry (Genty et al. 1989, Maxwell and Johnson 2000). Note that Y(II) effective is strongly correlated with the maximum quantum yield of PSII (e.g. Demming and Björkman 1987, Adams et al. 1995) commonly used as an indicator of both the leaf potential photosynthetic capacity and abiotic stresses (e.g. Kitajima and Butler 1975, Demming and Björkman 1987, Percival 2004, 2005, Galmés et al. 2007, Oukarroum et al. 2009, Guidi and Calatayud 2014).

We measured these leaf-level photosynthetic properties of Spathodea plants (1 m to 5 m in height) localized on the leeward coast of Tahiti Nui and Tahiti Iti. We report fluorescence results for leaves partially and fully in sun during measurements. A total of 50 Spathodea plants were measured in the field with 1 to 3 replicate leaves per individual. These leaf-level photosynthetic measurements were done at different elevations (Figure 1):

1. In order to provide a control of photosynthetic properties of Spathodea in presumed favorable conditions at low elevation, we selected some Spathodea plants (n = 10; < 125 m a.s.l.) located in suitable conditions (i.e. deep volcanic soil in the bottom of a valley with slope ≤ 5°, near a stream and not exposed to strong wind) on the leeward coast of Tahiti;

2. Along the Tahiti Nui elevational transect, accessible Spathodea plants (n = 26) were sampled between 180 m and 990 m elevation;

3. Finally, along a wetter elevational transect on the Peninsula of Tahiti Iti, accessible Spathodea plants (n = 14) were measured at elevations between 245 m and 850 m (Figure 1).

Along the elevational transect of Tahiti Nui (here after ETTN), we used stepwise regression to observe the relationship between the abundance of Spathodea against elevation and slope steepness in the 124 plots (XLStat® software v. 2009). Spathodea distribution was examined more closely by plotting frequency of Spathodea into elevation ranges. Frequency [0-1] was calculated by grouping number of Spathodea into elevation range from 140 to 1,300 m a.s.l.. We then divided the total number of Spathodea observed in each elevation range by the total of Spathodea counted along the elevational transect (n = 2,274). We assessed whether some elevation ranges are more or less frequently colonized by Spathodea.

Along the ETTN, the distribution of temperature, air humidity, and dew-point temperature in the elevation ranges of Spathodea was investigated in ten plots (Box plots, PAST® software v. 3.10). IButtons may experience some fluctuations in temperature and air humidity due to unpredictable periods of high light during sunflecks in the understory (Chazdon 1988, Canham et al. 1990, Pearcy et al. 1994). So, we provided all data for the night (no possible sunflecks from 8:00 pm – 4:00 am) and used interquartile ranges with Box plots to delete outliers and extreme values for the day (6:00 am – 6:00 pm). We then calculated average temperature and average air humidity for site by summing all daily measurements (based on a midnight-to-midnight day) for every day (n=84) and then dividing the total by the number of summed values. The highest and the lowest maximum temperature observed at the site was identified, and the same for the highest and the lowest maximum air humidity. The total number of values below the dew-point temperature (meaning condensation) was also investigated for every day (based on a midnight-to-midnight day) of the total data set and then converted into percent. We then used stepwise regression to observe the strongest relationships between micro-climate and abundance of Spathodea in the 10 plots fitted with iButtons (XLStat® software v. 2009).

Finally, ANOVA and the Dunnett test (XLStat® software v. 2009) were used to identify significant differences in photosynthesis responses of Spathodea (i.e. Fo’, ETR_max and Y(II)effective) between elevation ranges along the ETTN and between similar elevation ranges on the wetter Peninsula of Tahiti Iti.

A total of 2,274 Spathodea plants (≥ 3 m) was recorded along the ETTN. The Spathodea observed at the highest elevation was found at 1,240 m. Abundance of Spathodea decreased with increasing elevation (P < 0.0001, Figure 2a). Spathodea was observed on slope steepness ranging from 0.3° to 73.5° and its distribution was not influenced by the steepness (P = 0.95, Figure 2b). Within the elevation ranges of 140–540 m and 941–1,040 m the frequency of Spathodea was high, whereas it was less frequent between 541–940 m (Figure 3).

Figure 2.

Abundance of Spathodea (number of individuals) in relation to elevation (a) and slope steepness (b) in the 124 plots (ca. 200 m² per plot) along the elevational transect of Tahiti Nui.

Figure 3.

Frequency of Spathodea plants (n=2,271) along the 6.2 km transect from 140 to 1,300 m above sea level (a.s.l.) on the leeward coast of Tahiti Nui (Society Islands, French Polynesia). The increment of elevation range categories is 100 m, error bars refer to Standard deviation.

We provided average and extreme values of micro-climate for the 84 days surveyed from July to October in the data set (Table 1). Spathodea was found in an area with average July-October temperatures ranging from 24.5 °C (at 140 m) to 14.6 °C (at 1,241 m), whereas minimum and maximum temperatures ranged from 9.2 °C to 18.8 °C and 21 °C to 31.8 °C, respectively (Table 1). In Spathodea’s distributional range, average July-October air humidity was very high across all elevations ranging from 85.7 to 99.8%, whereas minimum air humidity values were observed at 653 m and ca. 900 m (Table 1, Figure 4a-d). Similarly, a lower percentage of values below the dew-point temperature (meaning poor condensation) was observed around 900 m elevation (Table 1). Thus, the elevation around 900 m seems to experience some air dryness along the ETTN. Among factors of micro-climate, the lowest July-October humidity and the lowest July-October temperature were significant in explaining variation observed in abundance of Spathodea in the 10 plots (Table 2).

Figure 4.

Box and whiskers plot. Temperature and air humidity recorded in 10 plots along the elevational transect between 140 and 1,300 m during 84 days of the dry season from July to October during night (a, b) and day (c, d) on the leeward coast of Tahiti Nui. Whiskers in the box plots show 95% of the data values.

At low elevation, under presumed low stress conditions, mean Chl fluorescence Fo’ was 75.8 µmol photons m^-2·s^-1 (Table 3). Mean ETR_max was 185.2 μmol electrons m^-2·s^-1 and the mean value of Y(II)effective was 0.52 relative units (Table 3). These values were targeted for comparison with values along the elevational transects.

No significant difference between ETR_max and Y(II)effective against elevation range was found on the wetter Peninsula of Tahiti Iti (Table 4; Figure 5e, f). Photosynthesis measurements of Spathodea at mid-high elevation on the Peninsula of Tahiti Iti were very similar to those observed at low elevation. On the Peninsula of Tahiti Iti, we only observed a significant difference in Chl fluorescence Fo’ between low elevation and the elevation range of 181–540 m (Table 4; Figure 5d).

Figure 5.

Comparison of photosynthesis measurements with ANOVA: low elevation (< 125 m) vs. 181–540 m, 541–940 m, and 941–990 m along the elevational transect on Tahiti Nui (a, b, c) and on the wetter Peninsula of Tahiti Iti (d, e, f). Error bars refer to Standard deviation.

Along the ETTN, photosynthesis measurements were different compared to those at low elevation. Chl fluorescence Fo’ increased by 14% while Y(II)effective and ETR_max decreased by 9.6% and 10%, respectively (Table 3). Chl fluorescence Fo’ was significantly high in the range of 541–940 m (Table 4, Figure 5a). Finally, both ETR_max and Y(II)effective decreased significantly in the ranges of 541–940 m and 941–990 m compared to low elevation (Table 4; Figure 5b,c).

Overall, our findings show that the alien tree Spathodea has a broad ecological range. As reported by Fosberg (1992), it can be viewed as an “aggressive species”. However, the abundance of Spathodea differed with elevation and this pattern seemed related to the lowest maximum temperature and humidity.

Along the ETTN, the elevation range between 140 m and 540 m was highly colonized by Spathodea. Average air humidity (around 95–99%) and average temperature of 24.5°–22.1° seems to provide suitable conditions for Spathodea establishment. In addition, at this elevation range of 140–540 m, the soil is both moist and thick and generally less exposed to strong wind (Larrue pers. obs.). Major invasion of Spathodea on the island of Tahiti is currently reported on the leeward (drier) coast, mainly at low and mid-elevation on the slopes of the northwestern valleys found above the main cities of the urban area of Papeete (Larrue 2008). This pattern might indicate a signal of introduction history rather than preferred ecological conditions because the most invaded valleys are also the ones where Spathodea has had a longer time to spread from adjacent cities and homegardens (Pouteau et al. 2015). Thus, major populations of Spathodea observed on the leeward coast of Tahiti may be related with the past land use and forest disturbance due to the relative proximity of urban areas, but the climate also provided suitable growing conditions.

Spathodea was also well represented at upper elevations between 940–1,040 m in less disturbed areas of native rainforests and cloud forest dominated by native and endemic trees such Metrosideros collina, Weinmannia parviflora, Glochidion spp., Alstonia costata, Coprosma taitensis, Myrsine spp., Fitchia nutans, and tree ferns Cyathea spp. (Florence 1986, 1993, Meyer 1996, 2010). At ca. 900 m elevation, the angiosperm flora comprises 44% of indigenous species and 15% endemic species, reaching 67% endemic species at 1,000 m (Blanchard 2013). Along the ETTN 82% of endemic species were found between 900–1,000 m. Abundances recorded along the ETTN indicate that Spathodea is able to spread in these forests with an average temperature of 16.8°C and high air humidity.

Abundance of Spathodea was lower in the 541–940 m elevation range along the ETTN, showing that this range was less frequently colonized. Minimum values of both air humidity and dew-point were recorded in this range indicating that this elevation experiences greater air dryness, especially ca. 900 m. Temperature and humidity patterns across Tahiti is not uniform even at the same elevation due to local contrast and diversity in topography of valleys, plateaus, and mountains (Doumenge, pers. com.). In addition, the land-sea breeze system and the foehn wind blowing on the leeward coast may affect the air humidity and temperature pattern (Méndez-Lázaro et al. 1995, Oliphant et al. 2001). However, details of how climate is affected by the land-sea breeze system, foehn wind, lifting condensation level, and the upper cloud limit set by the tradewind inversion are still very poorly documented on Tahiti.

At the highest elevation at which Spathodea was observed along the ETTN (1,241 m) average temperature was 14.6 °C with the lowest maximum temperature of 9.4 °C. Average humidity was 99.3% with lowest humidity of 84.2% and 77% of values below the dew-point temperature. So, this elevation was a very wet environment with a high frequency of condensation and potential supplemental water from fog. Despite high humidity, Spathodea was less abundant at the highest elevations ranging from 1,040 to 1,300 m. Decreasing temperature, with lowest maximum temperature around 9 °C may be a limiting stressor for Spathodea invasion at high elevation.

Invasion by tropical alien plants are probably limited in tropical montane cloud forests of French Polynesia due to the decreasing propagule pressure at increasing distances from urban areas as well as the decreasing in temperature with the increasing elevation (lapse rate) (Pouteau et al. 2013). In the context of global warming, mean annual temperature has increased by 0.0343 °C per year on Tahiti between 1958 and 2002 (Laurent et al. 2004). While the environmental lapse rate can differ slightly according to authors, it is often reported at 0.0058 °C.m^-1 (Baruch and Goldstein 1999). Considering the increasing temperature on Tahiti and this lapse rate, the current upper limit of Spathodea may increase by ca. 200 m in 2050 reaching ca. 1,450 m elevation as upper limit on the leeward coast. Thus, Spathodea is an important threat to native species currently and will likely be an even greater threat in the future; there is an urgent need to target this species for biological control.

While Y(II)effective of Spathodea observed at low elevation was the highest observed in the sample on Tahiti, Y(II)effective was everywhere below the optimum estimated at 0.84 (Genty et al. 1989). This suggests that photosynthesis rate of Spathodea during the dry season on Tahiti was not at the optimum potentially due to lower rainfall.

Among Spathodea plants surveyed, Y(II)effective and ETR_max were comparable from low elevation to mid-high elevation up to 850 m on the Peninsula of Tahiti Iti. This indicates that the potential photosynthesis rate of Spathodea may be similar from sea level until mid-high elevation on the Peninsula of Tahiti Iti.

Along the ETTN, Chl fluorescence Fo’, ETR_max, and Y(II)effective were similar in the elevation range of 181–540 m compared to low elevation. These results are indicative of a similar photosynthetic capacity of Spathodea plants from sea level until ca. 540 m along the ETTN. These findings are congruent with the high frequency of Spathodea plants observed in this range. This leads us to classify this elevation range as a preferred environment for Spathodea on the leeward coast of Tahiti.

In contrast, in the elevation range of 541–940 m Chl fluorescence Fo’ was significantly higher, potentially indicating unhealthy plants (Percival 2005, Nikolić et al. 2008) while ETR_max was low suggesting drought stress (Li et al. 2008). These results are supported by the significant decrease of Y(II)effective observed at this range showing that photochemical conversion decreases at 541–940 m compared to low elevation. Y(II)effective is often described as a valuable physiological indicator of water stress (e.g. Genty et al. 1989, Li et al. 2010) or a mild leaf drought stress due to a drop in air humidity (Bunce 1991). Authors have shown that the decreasing of leaf photosynthesis efficiency due to mild water stress was firstly related to the progressive closure of stomata, leading to a decreased rate of net photosynthesis (Medrano et al. 2002, Brestic and Zivcak 2013, Yordanov et al. 2003). Considering these results and the low frequency of Spathodea observed in the elevation range of 541–940 m, this range may be viewed as a non preferred environment for Spathodea along the ETTN. In addition, the low frequency of Spathodea observed in the elevation range of 541–940 m could be explained by greater competition from pre-existing vegetation or from other invasive species as Miconia calvescens also found along the ETTN. The reduced photosynthetic capacity of Spathodea observed in this range may also be related to punctual variation of air humidity and decreased supplemental water from fog drip during the dry season. In the elevation range 941–1,040 m, Chl fluorescence Fo’ was similar to that observed at low elevation indicating that Spathodea plant seems to be in similar health to those at lower elevation. Because of both the relative abundance of Spathodea in the elevation range 941–1,040 m and Chl fluorescence measurement supporting healthy Spathodea plants, we identified this range as a suitable environment for Spathodea. However, Y(II)effective was significantly less efficient compared to low elevation. Considering that air temperature is one of the key factors controlling carbon gain and the photosynthesis efficiency (Chen et al. 2003, Richardson 2004), the decrease inY(II)effective was possibly due to lower temperatures than those observed at low elevation.

Y(II)effective and ETR_max observed on the Peninsula of Tahiti Iti at mid-high elevation were greater compared to mid-high elevation along the ETTN. Both transects have similar ferralitic soils derived from weathering of the volcanic rocks as the basalt (Jamet 1987), but the main difference in environmental conditions between the leeward coast of Tahiti Iti and Tahiti Nui is that Tahiti Iti is wetter (air humidity and rainfall) than Tahiti Nui (Pasturel 1993, Laurent et al. 2004). Based on the rainfall map of Tahiti, the ETTN started in an area ca. 2,350 mm of mean annual rainfall, increasing up to ca. 3,500 mm vs. 3,000 mm to 5,000 mm year^-1 at similar elevations on the Peninsula of Tahiti Iti (Pasturel 1993). Furthermore, major populations of Spathodea are usually observed on the wet windward coast of tropical islands, e.g. Smith (1985) and Loope et al. (1992) reported major infestations along the valley of northern and eastern slopes of Oahu and Kauai as well as in almost every rainforest in East Maui (Hawaiian Islands). This suggests that total rainfall may be an important factor for Spathodea establishment at mid-high elevation, where sun irradiance and wind are important stressors (Laurent et al. 2004).