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Environmental factors associated with modular growth and flowering phenology of Baptisia bracteata Muhl. ex. Ell.

INTRODUCTION

Baptisia bracteata Muhl. ex. Ell. (Cream Wild Indigo = B. leucophaea) and its congener, B. alba (L.) Vent (White Wild Indigo = B. leucantha) (Fabaceae), coexist in savannas and prairies of Northeastern Illinois (Mohlenbrock, 2002; Swink and Wilhelm, 1994). B. bracteata has an earlier flowering period, and is shorter in stature, flowering, and seed yield compared to B. alba. This phenology may enable B. bracteata to reduce competition with B. alba (Haddock and Chaplin, 1982) and also infestation by Apion rostrum Say (Apionidae) which is a pre-dispersal seed predator of both perennials (Petersen et al., 2012).

In contrast to B. alba which typically bears a main stem that extends over 1m in height, B. bracteata grows to a height of about 0.3m and has a spread of over 0.5m in rhizomatous genets that project multiple arching ramets. B. bracteata blooms during May when the prairie is coming out of a winter's senescence, forming conspicuous clumps of ramets with pale yellow-flowering racemes among the emerging vegetation. In contrast, B. alba flowers during June. Bombus spp. are the major pollinators of the congeners although both show a minor degree of autogamy (Haddock and Chaplin, 1982). Pod inflation in both species indicates successful pollination.

Growth patterns and reproductive traits of perennial plants are known to be affected by selective pressures in the forms of herbivores (Ehrlen, 1995; Osada and Sugiura, 2006), pollinators (Fulkerson et al., 2012; Mendez and Diaz, 2001), seed predators (Cariveau et al., 2004; Ehrlen et al., 2012; Mduma et al., 2007; Petterson, 1994), and competition for physical resources (Chen et al., 2010; Dong et al., 2013; Sanchex-Humanes et al., 2011; Szymura and Szymura, 2013). Plants that reproduce by sexual reproduction and clonal growth, like B. bracteata, may benefit from both forms of reproduction (Hartnett and Bazzaz, 1985; Schmid et al., 1995). Sexual reproduction can produce phenotypes that promote persistence in a changing environment and seeds can be dispersed away from the parent plant. In contrast, clonal growth does not disrupt an adaptive genetic type and can offer to buffer against environmental risks, e.g., predation of a ramet does not eliminate the genet and joined ramets may share resources.

There is no evidence that B. bracteata is pollen-limited (Petersen et al., 2013). Larger genets, based on counts of ramets, produce more flowers, suggesting an importance of a larger floral display. However, for producing so many flowers, the legume yields few seeds. A change in ramet counts/genet over a 3-year period indicated declining growth with genet size, reflecting possible resource limitation in larger genets (Petersen et al., 2013). Seed predation by A. rostrum does not appear to be negatively correlated to the number of seeds matured. In the course of studying B. bracteata, the high variances in seeds matured/pod or pods inflated/genet among plants and across years have limited the scope of conclusions that could be drawn from short-term studies. This study involves a multi-year study of the patterns of growth and reproduction of B. bracteata with the objectives of identifying environmental factors governing the modular growth and flowering phenology of the legume.

METHODS

The study location was the reconstructed 7.4ha Russell Kirt Tallgrass Prairie located on the main campus of College of DuPage, IL. Reconstruction of the prairie plot began in 1984. Major grasses are big bluestem (Andropogon gerardii Vitman), prairie dropseed (Sporobolus heterolepsis Gray), and Indian grass (Sorghastrum nutans (L.) Nash). Data were collected during the years 2007-2013, except for year 2010. During this 6-year period, the prairie was burned once, March of 2012.

A concentric cluster of stems was assumed to be one individual genet of B. bracteata based on inspection of excavated plants not included in the study. Sampling of genets was the same across years and designed to examine advantages of genet size to pollination success and seed yield. Genet size was estimated by counts of ramets/genet, pollination success by genet counts of pods inflated/flower, nutritional allocation to flowering by genet counts of flowers/ramet, and seed yield by seeds matured/genet. Included with this analysis were flowering onset and duration, and infestation of pods by A. rostrum.

Genets of B. bracteata were randomly selected for study and each were counted for ramets, racemes, flowers, inflated pods, and seeds matured, date of onset of flowering, and flowering duration. Counts of A. rostrum/pod were also taken at the time of seed counts to estimate infestation rates. If pods had holes from which weevils could escape, A. rostrum were prorated from the total pod count using mean weevil counts of intact pods.

Thirty-two of the genets had continually been sampled from 2008 to 2013, excluding 2010. These genets were used to investigate how genet size was related to future growth.

Statistical analyses were done using Statistica 6 (Statsoft, 2001). Relationships among the reproductive parameters and weevil infestations were examined using Spearman Rank Correlation when assumptions of parametric testing could not be met (Zar, 1984).

Regression analysis was done to examine the effects of ramet count/genet on flower investment for a given year, and using the 32 plants followed from 2008 through 2013, on future genet growth. Ramet and flower counts were first log10(x+1) transformed prior to analyses to meet normality.

Coefficients of variation (CV) were compared between smaller B. bracteata and those larger. Based on ramet counts/genet, the 32 genets were divided approximately in half by size for each year prior to analysis. Finding that the distributions followed normal distributions, the grand mean CVs from smaller and larger genets were compared across years using 2-tailed dependent t-tests to investigate the relationship between genet size and CV.

RESULTS

Table 1 shows the variation in growth parameters of B. bracteata and infestation of pods by A. rostrum across the years of the study. Genets with more ramets produced more racemes and flowers (Table 2). During the majority of the years, more ramets were also linked to more pods inflated, an earlier onset of flowering, and a longer flowering duration. Nevertheless, more ramets did not translate to more seeds matured/genet or to weevil counts/pod. A greater floral display, based on raceme and flower counts per genet, was positively related pods inflated, and during some years, to seeds matured, but showed no relationship to weevil counts (Table 3). Similarly to ramet counts, plants with larger floral displays tended to flower earlier and for a longer duration. Pods inflated and seed matured per genet were always positively related to one another, and to counts of pods inflated/flower (Table 4). Only during two years of the study were the counts of pods inflated and A. rostrum/pod correlated, and positively. Counts of seeds matured/genet were never found to be related to the seed predator.

Larger genets yielded lower counts of flowers/ramet (Figure 1). In addition, the least growth in ramet counts/genet occurred among larger genets during 3 of the 4 sampling intervals and overall from 2008 to 2013 (Figure 2). Grand mean CV's computed across years was significantly greater for larger genets than those smaller (Table 5).

DISCUSSION

Expansion by B. bracteata through more ramets may enable establishment in a competitive environment. B. bracteata is short in stature among prairie vegetation to include among the tall grasses. After flowering, the legume remains green, presumably replacing energy and nutrient reserves needed for the next flowering season before senescing back to the soil at summer's end. Coverage of more space by a larger genet increases access to light, compensating to a degree for short height. We found little evidence that larger genets have higher pod inflation, yield more seeds, or attract more A. rostrum even though they tended to flower over a longer duration. Pod infestation rates by A. rostrum also failed to relate to counts of seeds matured/genet. The absence of correlations of weevil counts/ pod to inflated pods or seeds matured per genet could indicate that larger plants saturate the seed predator, or that ovipositing females mark pods, limiting the pod number of feeding larvae as has been shown by other weevils including Apion spp. (Hoddle, 1991; Kozlowski et al., 1983).

Stagnant to declining genet growth and counts of flowers/ramet, plus a higher CV in ramet counts among larger genets across years, indicate resources are becoming limited. Ramets of larger genets should be expected to suffer more unevenly from resource limitation than those smaller, resulting in a higher CV's for ramet counts. Although larger genets produced more racemes and flowers than those smaller, greater pod inflation and higher seed yield were occasional events mainly associated with the latter variables.

Trade-offs among components of reproductive yield are central to life history evolution (Roff, 1992). Increasing resource allocations to sexual reproduction or asexual reproduction can be at the expense of the other (Bazzaz et al., 1987; Cheplick, 1995; Ronsheim and Bever, 2000). Contrarily, larger size may enable plants to allocate more energy to both modes of reproduction (Coelho et al., 2005). We did not find clear evidence tradeoffs between sexual and asexual reproduction based on changing genet size. Larger genets despite producing more flowers, did so in decreasing proportion to size. The change in ramet growth also showed a negative relationship to genet size. With respect to growth pattern, B. bracteata appears to progress to a size limited by resources, with even the larger genets maturing a small but continuous number of seeds.

In conclusion, our results indicate that interspecific competition appears to be the force in selecting for larger genet size to the limits where resource limitation affects further growth. During some years, the size of inflorescence and flowering duration may function to promote flowers pollinated and seeds matured. Seed yield, which is small relative to flowers produced, may provide enough dispersal capability, plus the genetic variation needed to tolerate the unpredictable aspects of the tall-grass environment for even the larger genets constrained in expansion by resource limitation. Pre-dispersal seed predation by A. rostrum appears not to be so severe as to be related negatively to seed yield. Our findings do not discount the view that A. rostrum synchronizes it life cycle more around the prolific B. alba.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

received 1/30/14

accepted 8/10/14

LITERATURE CITED

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Mendez, M. and A. Diaz. 2001. Flowering dynamics of Arum italicum (Araceae): Relative role of inflorescence traits, flowering synchrony, and pollination context on fruit initiation. Am. J. Bot. 88:1774-1780.

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Petersen, C. E., S. M. Bauzys, F. A. Speranske, and B. A. Petersen. 2012. The varying phenology and growth patterns of Baptisia bracteata (Fabaceae) in reconstructed prairie. Trans. Ill. State Acad. Sci. 105:79-84.

Petersen, C. E., S. J. Detloff, S. K. Shukin, and B. A. Petersen. 2013. Does pollen limit seed set of Baptisia bracteata? Trans. Ill. State Acad. Sci. 106:1-8.

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Chris E. Petersen, Claira P. Mittman, Matt D. Mazur, Barbara A. Petersen

College of DuPage, Glen Ellyn, IL 60137
Table 1. Summary (mean [+ or -] 95% confidence limits) of
Baptisia bracteata growth parameters/genet and rates of Apion
rostrum pod infestations according to year of sampling. Except
where noted by subscript, sample sizes were 51 for 2007, 50 for
2008, 2009, and 2011, 53 for 2012, and 65 for 2013.

Parameter                      Year

                               2007

Ramets                   9.5 [+ or -] 1.9

Racemes                 5.55 [+ or -] 1.61

Flowers                   136 [+ or -] 47

Flowering            11.4 [+ or -] [1.4.sub47]
onset (days)

Flowering               14.5 [+ or -] 1.147
duration (days)

Pods inflated           41.6 [+ or -] 21.4

Seeds matured           45.1 [+ or -] 37.3

Apion rostrum/pod   0.99 [+ or -] [0.27.sub.39]

Inflated pods/      0.27 [+ or -] [0.08.sub.47]
flower count

Flowers/ramets           18.3 [+ or -] 8.3

Parameter                      Year

                               2008

Ramets                   8.0 [+ or -] 2.0

Racemes                 6.26 [+ or -] 1.91

Flowers                   114 [+ or -] 32

Flowering                9.7 [+ or -] 1.5
onset (days)

Flowering                16.8 [+ or -] 1.3
duration (days)

Pods inflated            9.8 [+ or -] 6.2

Seeds matured           28.1 [+ or -] 32.7

Apion rostrum/pod   O.43 [+ or -] [0.35.sub.20]

Inflated pods/          0.07 [+ or -] 0.03
flower count

Flowers/ramets           16.1 [+ or -] 2.7

Parameter                      Year

                               2009

Ramets                   9.6 [+ or -] 1.9

Racemes                 7.02 [+ or -] 1.57

Flowers                   95 [+ or -] 24

Flowering                9.2 [+ or -] 1.6
onset (days)

Flowering                17.2 [+ or -] 1.1
duration (days)

Pods inflated           32.3 [+ or -] 12.9

Seeds matured           62.5 [+ or -] 41.3

Apion rostrum/pod   0.28 [+ or -] [0.12.sub.32]

Inflated pods/          0.35 [+ or -] 0.12
flower count

Flowers/ramets           11.8 [+ or -] 2.7

Parameter                      Year

                               2011

Ramets                   10.7 [+ or -] 2.2

Racemes                 6.86 [+ or -] 2.92

Flowers                   105 [+ or -] 42

Flowering           14.0 [+ or -] [2.0.sub.42]
onset (days)

Flowering           16.5 [+ or -] [2.2.sub.42]
duration (days)

Pods inflated           23.0 [+ or -] 18.9

Seeds matured            7.2 [+ or -] 11.2

Apion rostrum/pod   0.83 [+ or -] [0.33.sub.24]

Inflated pods/        0.14 [+ or -] [0.06.sub.47]
flower count

Flowers/ramets           10.1 [+ or -] 3.2

Parameter                      Year

                               2012

Ramets                   13.6 [+ or -] 3.6

Racemes                 6.59 [+ or -] 2.24

Flowers                   100 [+ or -] 37

Flowering                9.2 [+ or -] 1.1
onset (days)

Flowering                13.4 [+ or -] 1.2
duration (days)

Pods inflated           48.8 [+ or -] 24.7

Seeds matured           30.3 [+ or -] 16.1

Apion rostrum/pod   0.32 [+ or -] [0.13.sub.43]

Inflated pods/          0.82 [+ or -] 0.09
flower count

Flowers/ramets           8.1 [+ or -] 1.9

Parameter                      Year

                               2013

Ramets                   13.6 [+ or -] 2.6

Racemes                 11.12 [+ or -] 2.30

Flowers                   160 [+ or -] 37

Flowering                2.8 [+ or -] 0.5
onset (days)

Flowering                18.1 [+ or -] 1.0
duration (days)

Pods inflated            21.6 [+ or -] 7.4

Seeds matured            9.9 [+ or -] 9.2

Apion rostrum/pod   0.55 [+ or -] [0.13.sub.49]

Inflated pods/          0.18 [+ or -] 0.06
flower count

Flowers/ramets           12.3 [+ or -] 2.2

Table 2. Spearman rank correlation comparing ramet counts to
those for growth parameters of Baptisia bracteata and Apion
rostrum/pod according to year. All counts are per genet except
for counts of the weevils which were weighted per pod of a genet.
Except where noted by subscript, sample sizes were 51 for 2008,
50 for 2007, 2009, and 2011, 53 for 2012, and 65 for 2013. Bold
type indicates significant (P < 0.05). Symbols for counts are
denoted Ra=racemes, Fl=flowers, PI=pods inflated, Se=seed
matured, and AR=A. rostrum. Fl On=flowering onset and Fl
Du=flowering duration.

Parameter   Year    Ra      Fl     PI      Se         AR

Ramets      2007   0.50#   0.33#   0.17    0.02    [0.20.sub.39]
            2008   0.55#   0.65#   0.15    -0.06   [0.00.sub.20]
            2009   0.45#   0.41#   0.43#   0.10    [-0.06.sub.32]
            2011   0.33#   0.35#   0.28#   0.24    [0.02.sub.24]
            2012   0.57#   0.54#   0.33#   0.24    [0.27.sub.43]
            2013   0.78#   0.33#   0.33#   0.13    [0.18.sub.49]

Parameter   PI/Fl            FlOn             FlDu

Ramets      [0.07.sub.47]   [-0.32.sub.47]#   [0.03.sub.47]
             0.09           -0.20             0.13
             0.20           -0.35#            0.36#
             0.21           -0.07             0.45#
            -0.07           -0.38#            0.49#
             0.33           -0.28#            0.31#

Note: The significant (P < 0.05) are indicated with #.

Table 3. Spearman rank correlation comparing counts of racemes
and flowers to those for growth parameters of Baptisia bracteata
and Apion rostrum/pod according to year. All counts are per genet
except for counts of the weevils which were weighted per pod of a
genet. Except where noted by subscript, sample sizes were 51 for
2008, 50 for 2007, 2009, and 2011, 53 for 2012, and 65 for 2013.
Bold type indicates significant (P < 0.05). Symbols for counts
are denoted by Fl=flowers, PI=pods inflated, Se=seed matured, and
AR=A. rostrum. Fl On=flowering onset and Fl Du=flowering
duration.

Parameter   Year    Fl      PI      Se           AR

Racemes     2007   0.91#   0.61#   0.23    [0.17.sub.39]
            2008   0.80#   0.32#   0.18    [0.27.sub.20]
            2009   0.83#   0.61#   0.27    [0.05.sub.32]
            2011   0.89#   0.52#   0.38#   [-0.14.sub.24]
            2012   0.93#   0.56#   0.40#   [0.21.sub.43]
            2013   0.92#   058#    0.16    [0.13.sub.49]
Flowers     2007           0.70#   0.31#   [0.18.sub.39]
            2008           0.21    0.00    [0.23.sub.20]
            2009           0.59#   0.20    [0.06.sub.32]
            2011           0.60#   0.49#   [-0.15.sub.24]
            2012           0.71#   0.43#   [0.27.sub.43]
            2013           0.66#   0.11    [0.20.sub.40]

Parameter   Year       PI/Fl            FlOn              FlDu

Racemes     2007   [0.12.sub.47]   [-0.55.sub.47]#   [0.33.sub.47]#
            2008       0.27             -0.22            0.20
            2009       0.25            -0.58#            0.42#
            2011       0.32#           -0.35#            0.50#
            2012       -0.04           -0.63#            0.63#
            2013       0.58#           -0.39#            0.42#
Flowers     2007   [0.20.sub.47]   [-0.42.sub.47]#   [0.28.sub.47]
            2008       0.11            -0.36#            0.37#
            2009       0.15            -0.55#            0.43#
            2011       0.37#           -0.32#            0.54#
            2012       0.10            -0.63#            0.66#
            2013       0.66#           -0.27#            0.32#

Note: The significant (P < 0.05) are indicated with #.

Table 4. Spearman rank correlation comparing counts of
pods inflated and seeds matured to those for growth parameters
of Baptisia bracteata and Apion rostrum according
to year. All counts are per genet except for counts
of the weevils which were weighted per pod of a genet.
Except where noted by subscript, sample sizes were 51
for 2008, 50 for 2007, 2009, and 2011, 53 for 2012, and 65
for 2013. Bold type indicates significant (P<0.05).
Symbols for counts are denoted by Se=seed matured, AR=A.
rostrum, PI=pods inflated, and Fl=Flowers. Fl On=
flowering onset and Fl Du=flowering duration.

Parameter   Year    Se           AR             PI/Fl         FlOn

Pods
inflated    2007   0.57#   [0.32.sub.39]#   [0.77.sub.47]#   -0.26
            2008   0.56#   [0.00.sub.20]        0.98#         0.00
            2009   0.52#   [-0.01.sub.32]       0.82#        -0.28
            2011   0.70#   [0.18.sub.24]        0.93#        -0.02
            2012   0.55#   [0.55.sub.43]        0.67#        -0.49#
            2013   0.48#   [0.19.sub.49]        1.00#        -0.13
Seed
matured     2007           [0.02.sub.39]    [0.54.sub.47]#   -0.17
            2008           [0.32.sub.20]        0.60#         0.23
            2009           [0.10.sub.32]        0.49#         0.02
            2011           [-0.11.sub.24]       0.61#         0.17
            2012           [0.12.sub.43]        0.33#        -0.24
            2013           [-0.01.sub.49]       0.48#         0.22

Parameter   Year   FlDu

Pods
inflated    2007   0.25
            2008   -0.06
            2009   0.52#
            2011   0.38#
            2012   0.48#
            2013   0.26#
Seed
matured     2007   0.24
            2008   -0.20
            2009   0.20
            2011   0.45#
            2012   0.24
            2013   0.07

Note: significant (P < 0.05) are indicated with #.

Table 5. Grand mean ([+ or -]
95% confidence limits) co-efficients
of variation (CV)
for ramet counts from
small and large genets
measured across the years,
2007, 2008, 2009, 2011,
2012, and 2013. Per year,
genet size was categorized
based on being below or
greater than the median
count of ramets/genet.
Grand means differed significantly (t=2.615; df=10;
P < 0.05).

Genet size     Mean [+ or -] SE

Small        0.390 [+ or -] 0.059
Large        0.485 [+ or -] 0.116
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Author:Petersen, Chris E.; Mittman, Claira P.; Mazur, Matt D.; Petersen, Barbara A.
Publication:Transactions of the Illinois State Academy of Science
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Date:Jan 1, 2014
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