Flowering phenology of South African Oxalis—possible indicator of climate change?

South African Journal of Botany 72 (2006) 150 – 156 www.elsevier.com/locate/sajb

Flowering phenology of South African Oxalis—possible indicator of climate change? L.L. Dreyer a,*, K.J. Esler b, J. Zietsman a a b

Department of Botany and Zoology, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa Department of Conservation Ecology, University of Stellenbosch, Private Bag x1, Matieland 7602, South Africa Received 8 March 2005; accepted 15 June 2005

Abstract Oxalis is a large geophytic genus that has diversified extensively in the winter rainfall region of the Cape Flora, South Africa. Patterns of flowering within Oxalis were investigated at both a regional scale (focusing on timing of flowering of Oxalis species in the Cape Region) and a local scale in a single habitat, the J.S. Marais Park, Stellenbosch, over 3 years (1999, 2003 and 2004). We found the active growth period of Oxalis to coincide with the peak rainfall period in the Cape Region, the start of flowering dependent on both the onset of the first significant rains and a drop in average daily temperatures. Both at a regional and local scale endospermous (dormant seed) species displayed an extended flowering season, while exendospermous (non-dormant seed) species displayed flowering peaks early in the rainy season. This correlates well with seedling strategies, in that dormant seeds of endospermous species are less affected by the dry summer months, while seeds of exendospermous species lack dormancy, and must thus germinate and establish seedlings well-before the onset of the dry summer months. Oxalis species in the local study displayed sequential replacement of flowering onset over the growing season, although there was an overlap in peak flowering times. The flowering sensitivity to alterations in temperature and delayed onset of winter rains suggests that specifically exendospermous species of Oxalis may indicate changes in climate. We hypothesize that global warming will influence the relative proportions of exendospermous vs. endospermous species flowering at local and regional scales in the Cape Region of South Africa. D 2005 SAAB. Published by Elsevier B.V. All rights reserved. Keywords: Oxalidaceae; Endospermy; Exendospermy; Phenophases

1. Introduction Oxalis L., consisting of almost 900 species, is the largest and most diverse genus within the Oxalidaceae. The genus displays two centers of diversity, one in southern Africa and the other in South –Central America. While the American species display a range of growth forms (annuals, geophytes, subshrubs, shrubs and trees), all southern African members of Oxalis are geophytes with true bulbs (Lourteig, 1994, 1995, 2000; Salter, 1944). In South Africa, 210 species (T 270 taxa) of Oxalis have been recorded (Dreyer and Makgakga, 2003) and it is the seventh largest genus within the Cape Flora (Goldblatt and Manning, 2000). Most of the southern African species of Oxalis are localized in the southern and southwestern parts (winter rainfall area) of the Western Cape Province, * Corresponding author. E-mail address: [email protected] (L.L. Dreyer).

forming a distinct centre of diversity in this region (Salter, 1944; Oberlander et al., 2002). Phenology is the study of the timing of recurring life cycle events and their relationship to seasonal climatic changes (Rathcke and Lacey, 1985). Flowering time ultimately influences plant success as this event has important implications for processes such as pollination and seed dispersal. While flowering time may be influenced by a range of selective factors such as climatic variation (Debussche et al., 2003), soil moisture (Struck, 1994), pollinator availability (Waser, 1979; Johnson and Bond, 1994) and conditions for recruitment (Pierce, 1984; Johnson, 1992b), there is evidence that, within lineages, flowering time may also be phylogenetically constrained (Johnson, 1992a). Johnson (1992a) investigated patterns of flowering in the Cape Flora in relation to rainfall seasonality and phylogenetic affinity, and suggested that strong differences in flowering times between some lineages (particularly in monocotyledons that produce single inflorescences)

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L.L. Dreyer et al. / South African Journal of Botany 72 (2006) 150 – 156

could be explained by the timing of other phenophase events such as seed dispersal and germination. Oxalis species display two distinct seed types and corresponding seed germination strategies. Species with endospermous seeds produce a thick, brown seed coat, enclosing varying amounts of endosperm around a small underdeveloped embryo (Fig. 1a–b). These seeds are thought to remain dormant during ensuing dry summer months and only germinate during cold wet winter months (Salter, 1944). Exendospermous seeds (Fig. 1c–d) are softer, with a translucent, membranous seed coat, through which the well-developed green embryo is clearly visible (Salter, 1944). At maturity, the elastic outer testa layer acts as an ejector. This layer ruptures via a split that develops on the adaxial side of the seed and the seed is explosively released from the capsule. The embryo germinates immediately and presumably forms a new bulb within the same growing season (Salter, 1944). The focus of this study was to investigate patterns of flowering within a single genus, Oxalis, at (1) a regional scale, focusing on timing of flowering of Oxalis species occurring in the Cape Region (Goldblatt and Manning, 2000) and (2) at a local scale and in a single habitat, the J.S. Marais Park, Stellenbosch, over 3 years (1999, 2003 and 2004). We asked the following questions: & Is there a general pattern in flowering of Oxalis species in the Cape Region? & Can flowering patterns be related to seed germination strategies? & Are there trends in flowering sequences?

151

& Can we, based on field observations, hypothesize a relationship between timing of flowering and climatic constraints (rainfall and temperature)? Based on these observations, we hypothesize how climate change might influence phenology and therefore the future status of Oxalis populations. It is valuable to identify these types of patterns, as understanding phenotypic responses to environmental variability and life history traits is an important step to predicting impacts of climate change. Model based predictions of climate change for Africa suggest that the continent will become alarmingly warmer (2 –6 -C) in the next 100 years (Hulme et al., 2001). At a regional scale, models are less accurate, but predictions for the Cape Floristic Region indicate that this area will become warmer and drier. Using the Global Circulation Model HadCM2, Bomhard et al., 2005 calculated an average increase in mean annual temperature for the Cape Floristic Region of 0.7 -C T 0.1 -C (range 0.5– 1.0 -C) and an average decrease in mean annual precipitation of 41 mm T 25 mm (range 7 – 295 mm) in the next 45 years. This change in climate is expected to have a range of consequences for biodiversity and a dramatic impact on the Cape Flora (Bond, 1997). In the last decade, changes in plant phenological patterns have been identified as sensitive and observable indicators of climate change. Most of the evidence comes from the northern latitudes (e.g. Le´vesque et al., 1997; Dunne et al., 2003; Aerts et al., 2004), although there have been some recent studies exploring the causes of variation in phenology from the

e

en t a

b

c

t

c

e

d

Fig. 1. Comparison of seed morphology and anatomy of selected endospermous (a – b) and exendospermous (c – d) Oxalis species. (a) Mature seed of O. grammopetala Sond. with hard, brown testa; (b) section through mature seed of O. corniculata L. showing an under-developed embryo and endosperm; (c) mature seed of O. hirta L. with split membranous testa and green cotyledons; (d) section through mature seed of O. xantha Salter showing a well-developed embryo with large cotyledons and no endosperm. c = cotyledon, e = embryo, en = endosperm, t = testa.

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Table 1 Oxalis species monitored in the J.S. Marais Park, Stellenbosch, South Africa Section

Subsection

Species

Cernuae Cernuae Cernuae Oppositae Oppositae Stictophyllae Sagittatae Angustatae Angustatae Angustatae –

Eu-cernuae Lividae Stellatae Subintegrae Subintegrae – – Sessilifoliatae Sessilifoliatae Lineares –

O. O. O. O. O. O. O. O. O. O. O.

pes-caprae L. livida Jacq. caprina L. obtusa Jacq. luteola Jacq. purpurea L. nidulans Eckl. and Zeyh. hirta L. tenuifolia Jacq. glabra Thunb. monophylla L.

Mediterranean region (Pen˘uelas et al., 2002; Debussche et al., 2003). Flowering in geophytic Mediterranean Cyclamen spp. is temperature dependent, above a minimum moisture threshold (Debussche et al., 2003). Pen˘uelas et al. (2002), using a long term data set from the Mediterranean, reported shifts in flowering dates and a lengthening of the plant growing season associated with an increase in annual average temperatures.

district. The mean annual rainfall in the Stellenbosch district over the past 30 years was 730 mm T 131.07 mm. Over this monitoring period, the average rainfall exceeded 100 mm/ month during May (104.9 mm), June (124.4 mm) and July (120.6 mm), while April (79.6 mm) and August (83.1 mm) also received significant amounts of rain. Total annual rainfall for 2003 (758.8 mm) exceeded the long-term average, while 1999 (556.3 mm) and 2004 (579.9 mm) were outlier years that were much drier (below one standard deviation of the mean). 2.4. Data analysis A chi-square analysis (Statistica Ver. 7) was used to determine if endospermous and exendospermous species display significantly different flowering distributions. To determine the relative effects of season (autumn, winter, spring and summer), rainfall and temperature on the number of Oxalis species flowering in the J.S. Marais Park, a regression tree analysis (Breiman et al., 1993) was conducted using CART (Salford Systems Ver. 5.0). 3. Results 3.1. Regional scale phenology

2.1. Regional scale phenology

Unlike the majority of species in the Cape Region which show a peak of flowering in spring (Johnson, 1992a; Pierce and Cowling, 1984), flowering of Oxalis in the Cape Region occurs from autumn to spring with a peak in late autumn to early winter (May and June). During the dry summer months (November to February), very few species flower (Fig. 2), and those that do, have ranges that extend into the summer rainfall regions of South Africa, e.g. O. tragopoda T.M.Salter, O. incarnata L. and O. smithiana Eckl. and Zeyh. Endospermous and exendospermous species display significantly different flowering distributions (v 2 = 177.0025, df = 11, p < 0.0001), with the bulk of the exendospermous species flowering during a marked peak earlier in the year (May and June), tailing off rapidly into spring and summer. In contrast, endospermous species flower over a more extended period ranging from mid-autumn to mid-spring. Proportionally, more

Flowering times of Oxalis species in the Cape Region were obtained from 5-year field observations, during which 736 Oxalis specimens (representing 150 Oxalis species) from across the region were collected from their natural habitats. These data were supplemented by PRECIS data and published accounts (Goldblatt and Manning, 2000). All species included in the Cape Region were incorporated in our analyses. We followed Salter (1944) in our demarcation of endospermous and exendospermous species. 2.2. Local scale phenology We studied the phenological patterns of 11 Oxalis species, representing six of the nine indigenous southern African sections (Table 1), in the J. S. Marais Park, an urban remnant of lowland Fynbos in Stellenbosch, South Africa. Populations were monitored once a week from April to October during 1999, 2003 and 2004. In 1999, only seven species were monitored, and no data were collected for O. caprina, O. luteola, O. livida and O. nidulans. During weekly visits, the species were assessed and assigned to one of the following three categories: (i) in bud, (ii) in flower and (iii) in fruit. Only the full dataset for 2004 is shown. Results were used to construct a phenogram for 2004, which was compared to one constructed from data collected in 2003 and in 1999.

No. of Oxalis spp. flowering (%)

2. Methods

100 Exendospermous

80

Endospermous 60 40 20 0 J

F

M

A

M

J

J

A

S

O

N

D

Month

2.3. Climatic measurements Daily temperature and precipitation records were obtained from the Nietvoorbij Weather Station in the Stellenbosch

Fig. 2. Flowering phenology of exendospermous (N = 97) and endospermous (N = 55) species of Oxalis that occur in the Cape Region. Data for each category are expressed as the percentage of the total species that are flowering in any 1 month.

L.L. Dreyer et al. / South African Journal of Botany 72 (2006) 150 – 156

153

% Oxalis spp flowering

100 90

1999

80

2003

70 2004

60 50 40 30 20 10

Oct 1 -1 0

Sep 1 -1 0

Aug 1 -1 0

Jul 1 -1 0

Jun 1 -1 0

May 1-10

Apr 1 -1 0

Mar 1 -1 0

Feb 1 -1 0

1 -1 0

Jan

0

Fig. 3. Total rainfall and average daily temperature recorded from January to October (1999, 2003 and 2004). Data obtained from the Nietvoorbij Weather Station in the Stellenbosch district.

endospermous species flower in the later part of the year (August to October), closer to the onset of the summer-dry season. 3.2. Local scale phenology In the J.S. Marais Park, flowering peaked in late autumn (April) and winter (May to July) (Fig. 4), after the onset of the winter rains and cool temperatures (Fig. 3), but before the peak rainfall between July and September. Regression tree analysis indicated that in autumn (March, April), spring (September, 1999

Rain Average temp. Min/Max temp.

30

100

25

80

20

60

15

40

10

20 0

5 35

120

2003

30

100

25

80

20

60

15

40

10

20

5 35

0 120

2004

30

100

25

80

20

60

15

40

10

20

5

0

1-10 11-20 21-31 1-10 11-20 21-28 1-10 11-20 21-31 1-10 11-20 21-30 1-10 11-20 21-31 1-10 11-20 21-30 1-10 11-20 21-31 1-10 11-20 21-31 1-10 11-20 21-30 1-10 11-20 21-31

Temperature °C

120

Jan

Total rain mm

35

October) and summer (November, December, January and February), the percentage of species flowering declined with an increase in temperature. In winter, the percentage of species flowering was substantially higher, but declined with an increase in rainfall (Fig. 5). Onset and duration of flowering (Fig. 4) as well as rainfall patterns (Fig. 3) varied remarkably between the 3 years in which phenology was monitored. In 1999, flowering of all species only started in mid-May, likely delayed by the late onset of the first rains in mid-April and the decline in temperatures in late May. In 1999, total rainfall was low throughout winter with heavy rains only starting in August.

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Fig. 4. Flowering of Oxalis species (%) in the J.S. Marais Park during 1999 (N = 7 species monitored), 2003 (N = 11) and 2004 (N = 11).

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L.L. Dreyer et al. / South African Journal of Botany 72 (2006) 150 – 156 1.0

the distinct sequence of flowering onset was remarkably consistent between years and differed only in terms of three species, O. livida, O. tenuifolia and O. nidulans. Onset and duration of flowering of individual species varied annually, probably as a consequence of fluctuations in temperature and rainfall. Some species (O. livida, O. monophylla, O. luteola and O. caprina) have very short flowering periods. All of these species also normally have distinct phenological phases in which profuse flowering is followed by seed production (Fig. 7). Other species (O. purpurea, O. pes-caprae, O. hirta, O. tenuifolia, O. glabra and O. obtusa) display much longer flowering periods (Figs. 6 and 7). Species known to be widespread and invasive, O. purpurea and O. pes-caprae, produce buds, flowers and seeds over many months (Figs. 6 and 7). The remarkably extended flowering period of O. purpurea and O. pes-caprae in 2003 may be explained by the evenly distributed rainfall throughout winter and well-into spring of that year. The peak flowering and seeding periods of O. hirta overlap, while all of the other species show a more distinct seeding period (Figs. 6 and 7).

0.9 0.8

% flowering

0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 -0.1 -0.2 winter; autumn, spring, summer; rain mm <= 27.4 min. temp. °C <= 12.1 autumn, spring, summer; min. temp. °C > 12.1

winter; rain mm > 27.4

Fig. 5. Regression tree analysis of frequency (%) of flowering of Oxalis species. Explanatory variables were season (autumn, winter, spring, summer), rainfall (mm) and mean minimum temperature (-C).

Despite the late rains, flowering was terminated by midSeptember. In contrast, flowering started very early in 2003, with the earliest flowering commencing at the beginning of April. Rain in this year fell during January and February, with the first heavy downpours and a drop in temperatures occurring at the end of March. There was good rainfall throughout the whole winter and spring period, and the percentage of species in flower remained high for a longer period than in either of the other 2 years. In 2004, the earliest flowering was recorded two weeks later in mid-April. Although rainfall started during March, it was less plentiful than in 2003 and the highest rainfall was recorded only towards the end of July, which is very late for the Cape Region. There was considerable overlap in the timing of flowering of the species monitored in the J.S. Marais Park (Fig. 6), although April 1-10

O. caprina O. monophylla O. luteola O. hirta O. livida O. purpurea O. pes-caprae O. nidulans O. tenuifolia O. glabra O. obtusa

May 11-20

21-30

1-10

June 11-20

21-31

1-10

4. Discussion While Pierce and Cowling (1984) suggested that the general spring flowering behaviour of geophytes in the southeastern Cape is a response to rainfall coinciding with higher temperatures, our data suggest that, for at least these geophytic species, the start of flowering is dependent on the onset of the first significant rains after a dry summer, as well as a drop in average daily temperature. Thus, Oxalis is one of few Cape Region genera that flower predominantly over the winter period. The active growth period of Oxalis thus coincides with the peak rainfall period. In a speciose July

11-20

21-30

1-10

August 11-20

21-31

1-10

11-20

21-31

September

October

1-10

1-10

11-20

21-30

11-20

21-31

1999 2003 2004 1999 2003 2004 1999 2003 2004 1999 2003 2004 1999 2003 2004 1999 2003 2004 1999 2003 2004 1999 2003 2004 1999 2003 2004 1999 2003 2004 1999 2003 2004

Fig. 6. Comparative flower phenology diagram for the Oxalis species in bud and/or flower in the J.S. Marais Park, Stellenbosch for 1999, 2003 and 2004.

L.L. Dreyer et al. / South African Journal of Botany 72 (2006) 150 – 156 April 1-10

11-20

May 21-30

1-10

11-20

June 21-31

1-10

11-20

July 21-30

O. caprina O. monophylla O. luteola O. hirta O. livida O. purpurea O. pes-caprae O. nidulans O. tenuifolia O. glabra O. obtusa

1-10

11-20

August 21-31

1-10

11-20

21-31

155

September 1-10

11-20

21-30

October 1-10

11-20

Bud Flow Seed Bud Flow Seed Bud Flow Seed Bud Flow Seed Bud Flow Seed Bud Flow Seed Bud Flow Seed Bud Flow Bud Flow Seed Bud Flow Seed Bud Flow Seed

Fig. 7. Details of bud, flowering and seeding phenology of the Oxalis species in the J.S. Marais Park, Stellenbosch for 2004. For flowering, dark shading indicates peak flowering periods (> 50% of the population), while lighter shading indicates a transition between phenophases and therefore reduced numbers of flowers (< 50% of the population).

environment such as the Cape Region, this type of asynchronous flowering surely has selective advantages, as competition for pollinators is reduced. Although the winter months are associated with a decline in pollinator activity (Pauw and Johnson, 1999), these species are serviced by generalist pollinators (Dreyer and Apinda-Legnouo, unpublished data). Further, should pollination fail in a given year, the geophytic nature and ability to reproduce vegetatively provides a buffer to population extinction. Salter’s (1944) and our own observations (Dreyer and Obone, unpublished data) have indicated that the amount of endosperm varies considerably in mature seeds of Oxalis, and might be linked to the timing and duration of seed formation. Exendospermous and endospermous species differ markedly in flowering patterns. Because endospermous species can display seed dormancy (Salter, 1944), there is less climatic constraint to seed survival and consequent germination. Seeds produced very late in the flowering season do not have to germinate and rapidly produce bulbs before the onset of the dry season. We observed an extended flowering season for this group of species that reached well into spring. In contrast, exendospermous seeds must germinate directly after release and are therefore constrained by the environment into which they disperse. We observed the majority of species to have a flowering peak early in the rainy season. At a local scale, our data also correlates with this trend. Endospermy, which represents the ancestral state in Oxalis, has been lost independently at least twice among southern African members of the genus based on trnL-F (Oberlander et al., 2004) and ITS sequence data (Oberlander, personal communication). Both exendospermous lineages show the same trend towards earlier flowering, suggesting that endospermy, and hence flowering time, is phylogenetically linked. These results also show that the switch to exendospermy is not phylogenetically constrained, as it has occurred more than once.

Of the species monitored at the local scale, O. caprina, O. livida, O. luteola, O. obtusa, O. pes-caprae and O. purpurea L. are endospermous, while O. glabra, O. hirta, O. monophylla, O. nidulans and O. tenuifolia are exendospermous. The extended budding, flowering and seeding periods of the weedy species O. pes-caprae and O. purpurea ties in well with their production of endospermous seeds that are able to go dormant until the next growing season. All of the exendospermous species completed their flowering and seeding by mid-winter, with the exception of O. glabra that reached peak seeding only towards the end of July and well into August (spring). Our observations of flowering sequences in the J.S. Marais Park suggest a sequential onset of flowering over the growing season, with minor variations in the sequence over the 3 years of monitoring, as has been observed by other authors (Pierce, 1984; Struck, 1994). Once flowering has commenced, however, there is a distinct overlap in flowering period of most of the species. Sequential flowering may enhance isolation barriers to prevent hybridization between species and/or to reduce competition for pollinators among species as suggested by Lieth (1971) and Pierce (1984). Synchronous flowering in Oxalis suggests the existence of other mechanisms for reproductive isolation. Further research is clearly needed on the periodicity of pollinators before we can fully evaluate their effects in controlling flowering sequences. This study, though covering only 3 years, shows evidence that warmer and drier years compress the flowering periods of Oxalis. The onset of flowering in this genus appears to be dependent both on a temperature decline and the onset of winter rains. During 1999, a year with below average rainfall, the onset and duration of flowering of Oxalis species in the J.S. Marais Park was dramatically delayed and shortened. In contrast, 2003 was an average year, and flowering commenced early and extended over a prolonged period. This sensitivity suggests that the genus, and more specifically exendospermous species, is potentially vulnerable to climate change. It is

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interesting to note that 57% of the red data species listed for Oxalis (Hilton-Taylor, 1996) are exendospermous. A shortened flowering period negatively affects the potential for sexual reproduction and, although the geophytic habit and the potential for vegetative reproduction of Oxalis could ensure survival from year to year (Bond, 1994), any restriction on sexual reproduction is potentially limiting in the longer term. Acknowledgements This project benefited from data collection by Inca Erasmus, Emelie Apinda-Legnouo and Charline Obone. We thank both the Subcommittee B of the University of Stellenbosch and the National Research Foundation (Gun: 2053585) for funding this project. Martin Kidd assisted with statistical analysis. Several unnamed referees are acknowledged for their improvements to the manuscript. References Aerts, R., Cornelissen, J.H.C., Dorrepaal, E., van Logtestijn, R.S.P., Callaghan, T.V., 2004. Effects of experimentally imposed climate scenarios on flowering phenology and flower production of subarctic bog species. Global Change Biology 10, 1599 – 1609. Bomhard, B., Richardson, D.M., Donaldson, J.S., Hughes, G.O., Midgley, G.F., Raimondo, D.C., Rebelo, A.G., Rouget, M., Thuiller, W., 2005. Potential impacts of future land use and climate change on the Red List status of the Proteaceae in the Cape Floristic Region, South Africa. Global Change Biology 11, 1452 – 1468. Bond, W.J., 1994. Do mutualisms matter? Assessing the impact of pollinator/disperser disruption on plant extinctions. Philosophical Transactions of the Royal Society of London. Series B 344, 83 – 90. Bond, W.J., 1997. Functional types for predicting changes in biodiversity: a case study in Cape Fynbos. In: Smith, T.M., Shugart, H.H., Woodward, F.I. (Eds.), Plant Functional Types: Their Relevance to Ecosystem Properties and Global Change. Cambridge University Press, Cambridge, pp. 174 – 194R ISBN 0-5215-6643-6. Breiman, L., Friedman, J., Olshen, R., Stone, C., 1993. Classification and Regression Trees. Chapman and Hall, New York. ISBN 0412048418. Debussche, M., Garnier, E., Thompson, J.D., 2004. Exploring the causes of variation in phenology and morphology in Mediterranean geophytes: a genus-wide study of Cyclamen. Botanical Journal of the Linnean Society 145, 469 – 484. Dreyer, L.L., Makgakga, M.C., 2003. Oxalidaceae. In: Germishuizen, G., Meyer, N.L. (Eds.), Plants of Southern Africa: An Annotated Checklist, Strelitzia, vol. 14. National Botanical Institute, Pretoria, pp. 174 – 194R ISBN 1-919795-99-5. Dunne, J.A, Harte, J., Taylor, K.J., 2003. Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecological Monographs 73, 69 – 86.

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