Informed Dispersal in Plants: Heterosperma Pinnatum (Asteraceae) Adjusts Its Dispersal Mode to Escape from Competition and Water Stress

Informed dispersal in plants: Heterosperma pinnatum (Asteraceae) adjusts its dispersal mode to escape from competition and water stress

Carlos Martorell and Marcela Mart í nez-L ó pez

C. Martorell ([email protected]) and M. Mart í nez-L ó pez, Depto de Ecolog í a y Recursos Naturales, Facultad de Ciencias, Univ. Nacional Aut ó noma de M éxico, Circuito exterior s/n, Ciudad Universitaria, 04510 M é xico, D.F., Mexico.

Informed-dispersal theory (IDT) states that organisms may use information on the quality of the local environment when deciding whether to disperse or not. Dispersal is expected to occur from adverse patches where the costs of philopatry (lack of dispersal) are greater than those of dispersal. Evidence of informed dispersal in plants is scarce, and experiments under natural conditions are lacking. We tested IDT in a semiarid grassland using the annual forb Heterosperma pinnatum , which produces awned, zoochorous achenes and unawned, philopatric ones. We expected the proportion of awned seeds to increase under adverse conditions that reduce fi tness, (i.e. under high competition and water stress). Heterosperma pinnatum was sown along natural moisture gradients with and without a shade that increased water availability. We found that competition (number of conspecifi c neighbors) and water stress reduced fi tness. As expected, the proportion of highly dispersible seeds increased under such conditions, probably as a strategy to escape from unsuitable patches. Many plants species do not behave as expected by IDT. Our results suggest that experiments under natural conditions in systems where the assumptions of IDT are met may prove to be a wealthy source of evidence for informed dispersal in plants.

Dispersal in space entails costs and benefi ts. It is necessary Informed dispersal in plants is well documented for veg- for species persistence, reducing competition, predation and etative propagation, but little is known about sexual repro- inbreeding, and allowing the recolonization of patches where duction. In many clonal species, new modules proliferate species become locally extinct. However, dispersal requires next to each other in resource-rich patches, but in poor con- energy and the development of expensive structures, and ditions long spacers (rhizomes, stolons) are produced so as migrants may fail to fi nd appropriate patches or experience to place the new modules as far as possible from the adverse high predation during dispersal (Olivieri and Gouyon 1997, patch (Lotscher 2006, Karban 2008, Lou â pre et al. 2012). A Ronce 2007, Bonte et al. 2012, Starrfelt and Kokko 2012). similar behavior would be expected for seeds: a plant’ s fi tness According to informed-dispersal theory, fi tness may be should increase if it was able to control the distance trav- increased if organisms use the information in their envi- eled by its propagules depending on the conditions of the ronment appropriately when deciding whether to disperse natal patch (McPeek and Holt 1992, Olivieri and Gouyon or not (Clobert et al. 2009, Bocedi et al. 2012, Starrfelt 1997, Bocedi et al. 2012). Seed dispersal is mostly passive, and Kokko 2012). Th e basis of this theory is that the bal- so it would appear that plants cannot control the distance ance between the costs and benefi ts of dispersal depends on traveled by their propagules. Th is is not the case: dispersal environmental conditions. In favorable patches, philopatry is aff ected by plant traits that have a high plasticity, such (i.e. lack of dispersal) may be benefi cial, whereas disper- as architecture (Donohue 1998), and wind-dispersed species sal from stressful areas should be favored because the costs may control the distance traveled by their seeds by modulat- of philopatry overcome those of leaving the natal patch. ing abscission according to wind speed (Soons and Bullock Dispersal is also expected in crowded patches where com- 2008). Yet other plants produce diff erent types of propagules petition is intense (McPeek and Holt 1992, Olivieri and with contrasting dispersal syndromes (Imbert 2002). In seed Gouyon 1997, Ronce 2007). Th us, informed dispersal heteromorphic (heterospermous) species, two or more dif- requires the acquisition of information on patch quality ferent types of seeds are produced, and fruit heteromorphic and neighbor density. Th at plants have such capability is (heterocarpous) plants produce diff erent kinds of fruits. becoming increasingly clear (Karban 2008, Novoplan- However, for simplicity, we will use the term seed hetero- sky 2009, Trewavas 2009). Th is suggests the possibility morphic species to refer to both. that informed dispersal is an adaptive behavior in plants Seed heteromorphic species are good candidates for (Bocedi et al. 2012). the evolution of informed dispersal because the distance

225 traveled by descendants may be easily regulated by produc- Awned achenes, however, are about 25% heavier due to the ing each type of propagule in diff erent proportions. Fur- weight of the awns and beak and have a higher survival rate. thermore, seed heteromorphic species produce diff erent No interannual seed bank exists for either type of achene types of propagules depending on the environmental con- (Venable et al. 1987). All these traits make H. pinnatum ditions (Baker and O’Dowd 1982, Cheplick 1987, Imbert an excellent system in which to study informed dispersal, and Ronce 2001, Brä ndel 2007, Culley and Klooster 2007), because selective pressures on achene type other than those suggesting the possibility that environmental information related to dispersal seem negligible. is used when allocating resources to produce philopatric or Th e study was conducted in Concepci ó n Buenavista, highly dispersible seeds. However, evidence for informed Oaxaca, Mexico (17° 53 ′ N, 97 ° 25 ′W, 2294 m a.s.l.). Th e dispersal has been found in just a few plants. Greater pro- vegetation is a short ( Ͻ 10 cm tall) grassland dominated by portions of highly dispersible propagules are produced Bouteloua spp. (Poaceae). Th e climate is cool and semiarid, in response to competition in Cakile edentula (Donohue with a mean temperature of 16.3° C, and an annual rainfall 1998, 1999), to competition and low nutrient availability in of 578 mm (mean of the three nearest stations, 4.5– 7.6 km Atriplex sagittata (Mand á k and Py š ek 1999), to water stress away from the study site). Th e soils are extremely thin, rarely and competition in Leontodon saxatilis (Br ä ndel 2007), and deeper than 20 cm, and develop over a pan of impermeable to nutrient defi cit in Crepis sancta (Imbert and Ronce 2001). tuff . Deeper soils retain moisture for longer, and thus are With the exception of the fi rst study, all the research has usually wetter (Villarreal-Barajas and Martorell 2009). Th e been conducted in controlled conditions. Apparently, the moisture gradient is evident in the vegetation, which is short behavior of seed heteromorphic plants may be quite diff er- and sparse in the dry, shallow soils. ent under fi eld and laboratory conditions (Mazer and Lowry 2003), so it is important to put informed dispersal to the test Experimental setup in natural conditions. In this paper we test the hypothesis that plants tend to In November 2010, all the capitula produced by over 40 escape from adverse patches and to remain in suitable ones H. pinnatum individuals were collected (1– 20 capitula by regulating the distance traveled by their seeds. To do per adult plant). Based on germination tests conducted in so, we use the species Heterosperma pinnatum (Asteraceae), January 2011, we found that awned achenes had greater an annual forb that produces two diff erent kinds of fruit germination rates, possibly because they loss dormancy two (achenes): some have awns and are amenable to dispersal by months earlier than unawned ones (Venable et al. 1987). animals, while others lack this structure and remain in the Th us, to have larger numbers of plants in our experiment, vicinity (Ͻ 20 cm) of the mother plant (Venable et al. 1987). we used only these achenes. To avoid biases due to maternal We assessed the eff ects of water stress and competition on fi t- or genetic eff ects, the achenes were pooled and mixed before ness and on the proportion of awned achenes produced. To sowing, thus warranting random allocation to the experi- do so, we set up a fi eld experiment in plots diff ering naturally mental treatments. in water availability and under shading that increased mois- In July 2011, at the beginning of the rainy season, we ture artifi cially. We expected a low fi tness and a large propor- selected 12 blocks (approx. 5 m2 each) in a fenced area tion of awned achenes in stressful and crowded patches. In that provided protection from livestock. In each block, fi ve contrast, unawned achenes would predominate in moist soils 10 ϫ 10 cm quadrats with soil depths of ca. 2, 4, 8, 15 and and in patches with a low density of conspecifi c neighbors. 28 cm were chosen. Th e exact depth was recorded in each quadrat by driving a metal rod into the soil until the tuff was reached. All the vegetation in each quadrat was removed Methods monthly. A mesh that reduced sunlight by 50% was placed in six randomly-chosen blocks. Th is treatment was expected Study species and site to increase soil moisture, and served the purpose of testing whether humidity (and not other soil attributes that might Heterosperma pinnatum is an annual forb some 7 cm tall at change with depth) was responsible for the changes observed the study site. It is heterocarpic: central fl orets tend to pro- in plants. If so, the responses observed when comparing sun- duce fruits with a long, awned beak that becomes attached lit and shaded areas would be similar to those recorded over to animal fur, and thus are transported over long distances. the depth gradient. Th ese achenes remain on the plant for longer periods, increas- Ten H. pinnatum achenes were sown at regular intervals ing the probability that they are picked up by mammals. inside a 7 ϫ 7 cm square within each quadrat to avoid com- Peripheral achenes are usually wider but shorter, lack awns, petition with plants at the periphery. We marked the exact and fall immediately after ripening. Th ese fruits, as well as position of each achene with a needle so we were able to tell awned achenes that are not dispersed by animals, remain in the seedlings coming from the achenes we sowed from those the vicinity (10 – 20 cm) of the parent plant (Venable et al. of naturally-occurring propagules. Th e latter were very rare, 1987). Unlike other seed heteromorphic Asteraceae, in which and were removed after emergence. At the end of the grow- disk (i.e. central) or peripheral fl orets can produce only one ing season, in November 2011, all the capitula on each indi- kind of achene, all H. pinnatum fl orets can produce either vidual were collected. We discarded a few that had already awned or unawned fruits (Venable et al. 1987). Th is releases dispersed some seeds. Th e number of awned and unawned the species from the indirect eff ects of capitulum size and achenes produced by each plant was recorded. from developmental constraints on the number of periph- To characterize moisture changes over the soil-depth gra- eral fl orets that characterize other species (Imbert 2002). dient and under the shades, we placed a GB-1 gypsum block

226 next to each quadrat and monitored it fortnightly with a soil Results moisture meter. Th e 2.5 cm long blocks were buried 1 cm in the soil. Th is precluded the collocation of blocks next to the Soil water potential increased with soil depth (from Ϫ 273 quadrats with 2-cm-deep soils. kPa in 2 cm soils to Ϫ 109 kPa in 28 cm soils under full sunlight; χ 2 ϭ 11.82, DF ϭ 1.76, p Ͻ 0.001), indicating that Statistical analyses stress was greater in the shallower soils. Shading further alle- viated stress (water potential was Ϫ 149 kPa in 2 cm soils and Changes in soil moisture with depth and shade were analyzed increased to Ϫ 60 kPa in 28 cm ones; χ 2 ϭ 40.92, DF ϭ 1 , with a generalized additive mixed model using sensor, block p Ͻ 0.001). Th e depth ϫ radiation interaction was not sig- and date as random variables (sensor nested in block, and nifi cant. both crossed with date), and log water-potential as response In full sunlight, the probability of reaching adulthood variable. Th is analysis was selected because the relationship increased with soil depth (from 0.11 in 2 cm to 0.22 in 34 between water potential and depth seemed non-linear. We cm, z ϭ 2.54, p ϭ 0.006). In the shade this probability was used package gamm4 (Wood 2012) in R. Signifi cance was larger (0.25 on average, z ϭ 3.16, p ϭ 0.001), although it measured through log-likelihood tests. decreased slightly in deeper soils (depth ϫ shade interaction We calculated the net reproductive rate, R 0, as an inte- z ϭ 2.14, p ϭ 0.016). Th e number of achenes produced per grative measure of fi tness. By defi nition R 0 is the number adult was greater in the shade than in full sunlight (z ϭ 3.54, of achenes produced per achene sown, so R 0 was calcu- p Ͻ 0.001) and decreased with competition (z ϭ 2.00, lated by multiplying the probability of becoming repro- p ϭ 0.022), especially in shallow soils (competition ϫ depth ϭ ϭ ductive by the average number of achenes produced by an interaction z 1.70, p 0.045). In sunlit plots, R 0 was large adult. Th e relationship between R0 and the proportion of in deep soils without competition (ca four achenes per sown awned achenes produced cannot be analyzed directly, as achene), whereas in shallow quadrats with greater competi- ϭ the proportion is undefi ned for plants that had an R0 0 . tion R0 was well below its equilibrium value of one (Fig. 1A). To solve this problem, we fi rst modeled the eff ects of In shaded plots R0 was 6– 8 times larger than in the sun. stress and competition on 1) the probability of any sown Depth had nearly no eff ect in the absence of neighbors, but achene to become reproductive, 2) the number of achenes the combined eff ect of competition and lack of water in shal- produced by reproductive plants, and 3) the proportion low soils reduced R 0 heavily (Fig. 1B). of awned achenes (see below for the statistical modeling As expected, the proportion of awned achenes increased procedures). We estimated R 0 as the product of fi rst and with competition (z ϭ 6.40, p Ͻ 0.001). Depth and light second models. Solving this system of equations, a rela- had a negligible eff ect on the type of achenes produced tionship between fi tness and proportion of awned achenes in the absence of competitors, but where competition can be calculated for diff erent soil depths and irradiance was intense much more awned achenes were produced in conditions. shallow soils compared to deep ones (competition ϫ depth To estimate the eff ects of stress on the probability of ger- interaction z ϭ 6.72, p Ͻ 0.001; Fig. 1C). Competition also minating and surviving to reproduction on soil depth and had a strong interaction with light (z ϭ 6.05, p Ͻ 0.001), shade, we regressed the fraction of seeds reaching adulthood as in general the fraction of awned achenes increased with on soil depth and shade using a generalized linear mixed competition in thin soils, but in the deeper portions of the eff ects model (GLME) using block as a random variable. We shaded blocks the opposite occurred (Fig. 1D). Note that we also regressed the total number of achenes per surviving indi- included in the models only those variables or interactions vidual on depth, shade and number of surviving neighbors that were signifi cant. as a measure of competition using a GLME using quadrat In general, the environmental conditions and competi- nested in block as a random eff ect (Crawley 2007, Gelman tion levels where R 0 was larger also resulted in the lowest and Hill 2007). Because of overdispersion when using proportion of awned achenes (compare left and right panels Poisson or binomial errors, data were transformed prior to in Fig. 1). Under full sunlight, there was a consistent reduc- fi tting and the residuals were visually checked for normal- tion in the production of zoochorous propagules as fi tness ity using q-norm plots. Th ese analyses were performed on increased. Th e same happened when radiation was reduced, package lme4 (Bates et al. 2011) for R. Th e probabilities of but only in shallow soils; where soil depth was greater than survival and the number of achenes produced were estimated 16.2 cm, the opposite pattern was observed (Fig. 2). Th is was for diff erent soil depths, shade level and competition inten- clearly the result of the already noted increase in the produc- sity using the two regression models described above, and tion of philopatric achenes with competition in deep, shaded multiplied to estimate R 0 . Finally, the proportion of awned soils (Fig. 1D) achenes was also regressed on depth, shade, and number of individuals in the quadrat. Th is analysis was performed using a GLME with quadrat nested in block as random variables, Discussion a binomial error and a logit link function. We expected fi t- ness measures (probability of reproducing and number of Th e behavior of Heterosperma pinnatum under natural con- achenes produced) to increase with soil depth and shade, and ditions matched closely that expected by informed-dispersal to decrease with the number of neighbors. Th e proportion of theory: this plant produced a greater proportion of highly awned achenes was expected to follow the opposite patterns. dispersible seeds where fi tness was at its lowest, i.e. in stress- To test these one-tailed tests we used the z-values provided ful environments and in the presence of competitors. Also by lme4. in accordance with our hypotheses, shading reduced stress,

227 R Net reproductive rate ( 0) Proportion

0 5 10 15 0.3 1 34 (A) (C)

34 (B) (D) Soil depth (cm)

2 05100510 Competition (number of neighbors)

Figure 1. Fitness (net reproductive rate) and investment in long-distance dispersal propagules (proportion of awned achenes) depending on competition, soil depth, and irradiance. Models for full sunlight (A, C) and shade (B, D) are shown. Note that under conditions that result in low fi tness (dark colors, left panels) more awned achenes are produced (light colors, right panels) except for the competition axis under shades, for which the pattern is reversed. increased fi tness, and enhanced the proportion of unawned However, the overall negative correlation between fi t- seeds. Th is, altogether with the fact that the assumptions of ness and proportion of awned seeds was not found in deep, the theory are likely to be met, suggests that H. pinnatum shaded soils: under such conditions, plants in crowded uses information about patch quality and competition to patches produced a greater proportion of philopatric seeds adjust its dispersal kernel. compared to individuals growing in low-density quadrats. Plant performance in drylands is strongly determined by Th e trend could appear to be maladaptive at a fi rst glance water availability (Noy-Meir 1973). Heterosperma pinnatum conforms to this pattern, as there was a close match between 1" soil moisture and fi tness. At the study site, competition has been found to increase in shallow soils, possibly because 0.75" water is scarcer (Villarreal-Barajas and Martorell 2009). Th is may explain why water stress was not very detrimental in the 0.5" absence of competitors. According to the theory, dispersal should be favored 0.25" under adverse conditions that reduce fi tness (Clobert et al. 2009, Bocedi et al. 2012, Starrfelt and Kokko 2012). Our 0" Proportion of awned achenes results support this idea, as H. pinnatum produced greater 0" 5" 10" 15" R proportions of awned achenes in patches where fi tness was Net reproductive rate ( 0) lowest. Even the relative insensitivity of fi tness to soil depth Figure 2. Relationship between fi tness (R 0 ) and proportion of in the absence of competitors was mirrored by the plant’ s awned achenes for diff erent environmental conditions. Colors production of diff erent achene types. Moreover, nearly every correspond to soil depth: light gray: 2 cm; dark gray: 18 cm; black: Ͻ achene produced in patches where R 0 1 had awns, i.e. 34 cm. Continuous line: full sunlight. Dashed line: shade. Th e where absolutely no benefi t can be obtained by producing models are graphed along the interval of R 0 values expected for philopatric progeny. each condition.

228 as competition reduced fi tness by ∼40%, so dispersing from (Yamaguchi et al. 1990). If hormones that are produced as crowded patches could potentially be appropriate. Nev- a result of stress promote the production of highly dispers- ertheless, according to informed dispersal theory, awned ible seeds, the cost of acquiring information on patch quality achenes would be produced only if the costs of competition would be quite low (assumption four). overcome those of dispersal (Clobert et al. 2009, Bocedi et al. 2012, Starrfelt and Kokko 2012). Despite the reduc- Informed dispersal in plants: an exception? tion in fi tness caused by competition in deep, shaded soils, R 0 was still much higher (nearly thrice as large) than the Seed heteromorphism has exerted a strong attraction for best-case scenario under the widespread full-irradiance ecologists, and research on the production of diff erent types conditions where awned achenes may be expected to land. of propagules depending on environmental conditions has Philopatric achenes may be produced because the levels of been extensive. In most cases, a greater proportion of philo- fi tness in deep, shaded soils are high enough to make the patric propagules is produced under adverse conditions cost of dispersal higher than the cost of staying and compet- (Koller and Roth 1964, Campbell et al. 1983, Cheplick ing (Ellner and Shmida 1981). Moreover, the production of 1987, Yamaguchi et al. 1990, Ruiz de Clavijo and Jim é nez awned achenes can be seen as an altruistic behavior (Ronce 1998, Culley and Klooster 2007). Why does the ‘ good-stay, 2007) that favors neighbors that produce only philopatric bad-disperse ’ rule appear to be so rare? achenes because they would enjoy the benefi ts of competi- In many of the species that have such unexpected behav- tion reduction without paying the costs of dispersal. Th ese ior, dispersal capability is confounded with other traits such ‘ free riders ’ would be especially favored in extremely favor- as propagule size (Cheplick 1987, Culley and Klooster 2007), able patches such as shaded plots with deep soils. Free riding the probability that seedlings root successfully (Cheplick may account for the reduction in the average proportion of and Sung 1998), developmental constraints (Ruiz de Clavijo awned achenes such plots even if this leads to a reduction in and Jimé nez 1998, Imbert and Ronce 2001), bet-hedging group fi tness (Rankin et al. 2007), and is perhaps an evolu- strategies (Venable 1985, Cheplick and Sung 1998), and tionary stable strategy. the sexual or asexual origin of the seed (Cheplick 1987, Heterosperma pinnatum behaves as predicted by the Culley and Klooster 2007). Th ese species are not appropriate informed-dispersal theory seemingly because all the theo- to test the predictions of informed-dispersal theory because ry ’ s assumptions are met. Informed dispersal is expected to the distance traveled by seeds may be the indirect result of evolve if 1) there are diff erences in patch quality in the envi- selective pressures on unrelated propagule-traits. In species ronment, 2) the future environmental conditions in a patch such as Cakile edentula, dispersal is aff ected by plant traits are predictable, 3) individuals are able to gather information such as size or architecture that are subject to selection them- about patch quality, and 4) the costs of information acquisi- selves. Furthermore, such attributes are highly plastic and, tion are low in comparison with the costs of making an uni- through maternal eff ects, may establish complex sets of cor- formed decision on whether to disperse or not (Ronce 2007, relations between the phenotypes of maternal and progeny Clobert et al. 2009, Bocedi et al. 2012). Th e fi rst condition is generations (Donohue 1998, 1999). Such phenomena are clearly met in our system, where plots diff er in water poten- likely to be common among plant species, and may hinder tial and in the fi tness of the plants that grow in them. Patch or even preclude the evolution of informed dispersal. conditions are also highly predictable: soil depth (and thus In other species the assumptions of informed dispersal diff erences in local water potential relative to other patches) are not met. In many cases the future environment is unpre- is expected to remain nearly constant over time. Future com- dictable (Venable 1985, Cheplick 1987, Cheplick and Sung petition may also be predictable from current plant density. 1998), so there is no reason to expect plants to behave as It is likely that only a few seeds are actually transported by expected by the theory (Bocedi et al. 2012). Th e very fact animals, and that most of them remain in the vicinity of that informed dispersal requires spatial heterogeneity may the mother plant. Th us, a currently high-density patch may hamper its evolution in some environments. Unlike animals, remain crowded in the future as well. plants do not search actively for favorable microsites. Th is Plants gather information about their habitat, and raises the costs of dispersal, especially in environments where thus are likely to fulfi ll the third assumption of informed- most of the area is unsuitable for establishment. In such hab- dispersal theory. Plants detect the roots of neighboring itats, the probability of reaching a safe site at random would individuals, and thus may assess plant density in their vicin- be extremely low, and plants may fi nd it more profi table to ity (Cahill and McNickle 2011). Such information is a clue invest in philopatric propagules (Ellner and Shmida 1981, to the competitive intensity in a patch. When it comes to Cody and Overton 1996, Cheptou et al. 2008). Many seed environmental stress, as in our case, the metabolic status of heteromorphic species from severe environments seem to the individual may also be highly informative about patch follow this ‘ pessimistic ’ strategy, and only invest in dispersal quality. Most plants show the same responses when grown if surplus resources are available (Cheplick and Quinn 1982, under stressful conditions, such as increased abscisic acid Cheplick 1987). (ABA) or reactive oxygen species concentration (Cruz de However, the scarcity of reports on informed dispersal in Carvalho 2008). Heterosperma pinnatum individuals growing plants may in part be due to the predominance of experi- in shallow soils would be expected to have greater amounts ments under controlled conditions and to species selection. of such compounds, which may then trigger the production In the dune annual Spergularia marina, Mazer and Lowry of awned achenes. Increased ABA concentration as a result (2003) report an apparently strong case for informed dis- of environmental stress regulates the production of diff erent persal in the fi eld that could not be confi rmed in the green- kinds of fruits in the heterocarpic species Salsola komarovii house. Th eir results indicate that the conditions required for

229 the production of highly dispersible fruits were hard to simu- Cheptou, P.-O. et al. 2008. Rapid evolution of seed dispersal in an late. Dispersal is also infl uenced by a myriad of plant traits urban environment in the weed Crepis sancta . – Proc. Natl that change under greenhouse conditions (Donohue 1998, Acad. Sci. USA 105: 3796 – 3799. 1999), and thus preclude the realistic study of informed dis- Clobert, J. et al. 2009. Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured persal. Th e failure to identify and reproduce experimentally populations. – Ecol. Lett. 12: 197 – 209. the specifi c environmental cues that trigger dispersal may be Cody, M. L. and Overton, J. M. 1996. Short-term evolution of responsible for the paucity of reports about informed dis- reduced dispersal in island plant populations. – J. Ecol. 84: persal in plants. On the other hand, studies may be biased 53 – 61. towards species that are appealing because propagules are Crawley, M. J. 2007. Th e R book. – Wiley. very diff erent. It is likely that in these cases the propagules Cruz de Carvalho, M. H. 2008. Drought stress and reactive oxygen vary in several traits besides dispersal capability, and thus species: production, scavenging and signaling. – Plant Signal- may be subject to many selective pressures. Th is is not the ing Behav. 3: 156 – 165. Culley, T. M. and Klooster, M. R. 2007. Th e cleistogamous breed- case in H. pinnatum , because awned and unawned achenes ing system: a review of its frequency, evolution and ecology in diff er mainly in the distance they may travel (Venable et al. angiosperms. – Bot. Rev. 73: 1 – 30. 1987). Informed dispersal has not been tested in plants that Donohue, K. 1998. Maternal determinants of seed dispersal in regulate their dispersal kernels without producing very dif- Cakile edentula: fruit, plant and site traits. – Ecology 79: ferent propagules, which may be far more common than 2771 – 2788. usually thought (Donohue 1998, Soons and Bullock 2008). Donohue, K. 1999. Seed dispersal as a maternally infl uenced Developmental constraints on the production of diff erent character: mechanistic basis of maternal eff ects and selection kinds of propagules are another source of confusion that is on maternal characters in an annual plant. – Am. Nat. 154: 674 – 689. not present in our species. Th e fraction of awned achenes Ellner, S. and Shmida, A. 1981. Why are adaptations for long- produced is extremely plastic. We found individuals that range seed dispersal rare in desert plants? – Oecologia 51: produced anything from exclusively awned achenes to philo- 133 – 144. patric propagules only. Experiments performed under natu- Gelman, A. and Hill, J. 2007. Data analysis using regressio ral conditions with species whose seeds diff er essentially in and multilevel/hierarchical models. – Cambridge Univ. their dispersal kernels may prove to be a wealthy source of Press. evidence for informed dispersal in plants. Imbert, E. 2002. Ecological consequences and ontogeny of seed heteromorphism. – Persp. Plant Ecol. Evol. Syst. 5: 13 – 36. Acknowledgements – PAPIIT-UNAM project IN225511 provided Imbert, E. and Ronce, O. 2001. Phenotypic plasticity for dispersal funding. Ver ó nica Zepeda, Alba Navarrete, Alejo Torres, LFVV ability in the seed heteromorphic Crepis sancta (Asteraceae). Boullosa, Diego Garc í a and Daniel Manzur assisted us in the fi eld – Oikos 93: 126 – 134. and lab. J. M. Bullock provided valuable insights that improved this Karban, R. 2008. Plant behaviour and communication. – Ecol. paper. Este trabajo fue posible gracias al invaluable apoyo de la Lett. 11: 727 – 739. comunidad de Concepci ó n Buenavista. Koller, D. and Roth, N. 1964. Studies on the ecological and physiological signifi cance of amphicarpy in Gymnarrhena micrantha (Compositae). – Am. J. Bot. 51: 26 – 35. Lotscher, M. 2006. Resource allocation in clonal plants. – Progr. References Bot. 67: 536 – 561. Lou â pre, P. et al. 2012. How past and present infl uence the forag- Baker, G. A. and O’Dowd, D. J. 1982. Eff ects of parent plant ing of clonal plants? – PLoS ONE 7: e38288. density on the production of achene types in the annual Mand á k, B. and Py š ek, P. 1999. Eff ects of plant density and Hypochoeris glabra . – J. Ecol. 70: 201 – 215. nutrient levels on fruit polymorphism in Atriplex sagittata . Bates, D. et al. 2011. lme4: Linear mixed-eff ects models using S4 – Oecologia 119: 63 – 72. classes. – R package. Mazer, S. J. and Lowry, D. E. 2003. Environmental, genetic and Bocedi, G. et al. 2012. Uncertainty and the role of information seed mass eff ects on winged seed production in the heteromor- acquisition in the evolution of context-dependent emigration. phic Spergularia marina (Caryophyllaceae). – Funct. Ecol. 17: – Am. Nat. 179: 606 – 620. 637 – 650. Bonte, D. et al. 2012. Costs of dispersal. – Biol. Rev. 87: 290 – 312. McPeek, M. A. and Holt, R. D. 1992. Th e evolution of dispersal Br ä ndel, M. 2007. Ecology of achene dimorphism in Leontodon in spatially and temporally varying environments. – Am. Nat. saxatilis . – Ann. Bot. 100: 1189 – 1197. 140: 1010 – 1027. Cahill, J. F. and McNickle, G. G. 2011. Th e behavioral ecology of Novoplansky, A. 2009. Picking battles wisely: plant behaviour nutrient foraging by plants. – Annu. Rev. Ecol. Evol. Syst. 42: under competition. – Plant Cell Environ. 32: 726 – 741. 289 – 311. Noy-Meir, I. 1973. Desert ecosystems: environment and Campbell, C. S. et al. 1983. Cleistogamy in grasses. – Annu. Rev. producers. – Annu. Rev. Ecol. Syst. 4: 25 – 51. Ecol. Syst. 14: 411 – 441. Olivieri, I. and Gouyon, P.-H. 1997. Evolution of migration Cheplick, G. P. 1987. Th e ecology of amphicarpic plants. – Trends rate and other traits. Th e metapopulation eff ect. – In: Ecol. Evol. 2: 97 – 101. Hanski, I. A. and Gilpin, M. E. (eds), Metapopulation Cheplick, G. P. and Quinn, J. A. 1982. Amphicarpum purshii and biology: ecology, genetics and evolution. Academic Press, the “ pessimistic strategy” in amphicarpic annuals with subter- pp. 293 – 323. ranean fruit. – Oecologia 52: 327 – 332. Rankin, D. J. et al. 2007. Th e tragedy of the commons in Cheplick, G. P. and Sung, L. Y. 1998. Eff ects of maternal nutrient evolutionary biology. – Trends Ecol. Evol. 22: 643– 651. environment and maturation position on seed heteromor- Ronce, O. 2007. How does it feel to be like a rolling stone? Ten phism, germination, and seedling growth in Triplasis purpurea questions about dispersal evolution. – Annu. Rev. Ecol. Evol. (Poaceae). – Int. J. Plant Sci. 159: 338 – 350. Syst. 38: 231 – 253.

230 Ruiz de Clavijo, E. and Jimé nez, M. J. 1998. Th e infl uence Venable, D. L. 1985. Th e evolutionary ecology of seed hetero- of achene type and plant density on growth and biomass morphism. – Am. Nat. 126: 577 – 595. allocation in the heterocarpic annual Catanache lutea Venable, D. L. et al. 1987. Th e ecology of seed heteromorphism in ( Asteraceae). – Int. J. Plant Sci. 159: 637 – 647. Heterosperma pinnatum in central Mexico. – Ecology 68: 65 – 76. Soons, M. B. and Bullock, J. M. 2008. Non-random seed Villarreal-Barajas, T. and Martorell, C. 2009. Species-specifi c abscission, long-distance wind dispersal and plant migration disturbance tolerance, competition and positive interactions rates. – J. Ecol. 96: 581 – 590. along an anthropogenic disturbance gradient. – J. Veg. Sci. 20: Starrfelt, J. and Kokko, H. 2012. Th e theory of dispersal under 1027 – 1040. multiple infl uences. – In: Clobert, J. et al. (eds), Informed Wood, S. 2012. gamm4: Generalized additive mixed models using dispersal and spatial evolutionary ecology. Oxford Univ. Press, mgcv and lme4. – R Graphic manual. pp. 19 – 28. Yamaguchi, H. et al. 1990. Diversities in morphological character- Trewavas, A. 2009. What is plant behaviour? – Plant Cell Environ. istics and seed germination behavior in fruits of Salsola 32: 606 – 616. komarovii . – J. Plant Res. 103: 177 – 190.

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