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Keywords:

  • exaptation;
  • feeding trials;
  • gut passage;
  • megafaunal dispersal syndrome;
  • Nicaragua;
  • physical dormancy;
  • surrogate dispersers;
  • tropical dry forest

Abstract

  1. Top of page
  2. AbstractResumen
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. Literature Cited
  9. Supporting Information

Endozoochory and fire are crucial ecological factors determining germination success and recruitment in many plant species. Fire is a well-known germination trigger while endozoochory may allow seed dispersal along with an increase in germination. Their interaction has rarely been addressed, however, even though both factors are pervasive in human-transformed ecosystems like most Neotropical Dry Forests (NDF). For three common Mesoamerican tree species (Acacia pennatula, Enterolobium cyclocarpum, and Guazuma ulmifolia), we used feeding trials to assess the preference of cattle, which are their main seed dispersal agent. We also experimentally tested the interaction between gut passage and fire as triggers of germination. The fruits of the three species were eaten by cattle, but the small seeds of G. ulmifolia were ingested 10-fold more than those of the other species. While gut passage did not have any effect on germination, heat-shocks above 90 °C increased the number of germinating seeds by 15 percent. These results suggest that cattle may be a key dispersal vector in NDF, but that fire may be an important germination trigger. Physical dormancy in these species may have been selected for by extinct megaherbivores because it was a key trait ensuring seed survival after gut passage. However, in light of the recent expansion of cattle-ranching and fire occurrence in NDF, it has become a useful exaptation facilitating the colonization of disturbed areas.

Resumen

La endozoocória y el fuego son factores ecológicos cruciales que determinan la germinación y el reclutamiento de muchas especies de plantas. El fuego es un conocido desencadenante de la germinación mientras que la endozoocória puede permitir la dispersión de semillas junto con un incremento en la germinación. No obstante, su interacción apenas ha sido abordada a pesar de que ambos factores son habituales en ecosistemas transformados por los humanos como la mayoría de los bosques secos neotropicales (NDF). En tres especies Mesoamericanas comunes (Acacia pennatula, Enterolobium cyclocarpum, Guazuma ulmifolia), evaluamos las preferencias del ganado, su principal agente dispersor, mediante ensayos de cafetería, y testamos la interacción entre endozoocória y fuego mediante un experimento en el cual el tránsito intestinal fue reproducido experimentalmente y seguido de golpes de calor que difirieron en temperatura y tiempo. Los frutos de las tres especies fueron consumidos por el ganado pero el menor tamaño de semilla de G. ulmifolia produjo una ingestión de semillas diez veces mayor. No hubo interacción entre tránsito intestinal y fuego: mientras que el primer factor no tuvo ningún efecto, golpes de calor por encima de 90 °C estimularon la germinación produciendo incrementos de hasta el 15% en el número de semillas germinadas. Estos resultados sugieren que el ganado puede ser un vector de dispersión clave mientras que el fuego puede ser un desencadenante de la germinación en los NDF. La dormición física en estas especies fue probablemente seleccionada por la megafauna extinta al ser este un atributo clave que aseguraba la supervivencia de las semillas tras el tránsito intestinal, pero a la luz de la reciente expansión de la ganadería y del fuego en los NDF, se ha convertido en una útil exaptación que facilita la colonización de áreas perturbadas.

Neotropical dry forests (NDF) are one of the most diverse but threatened ecosystems in the world (Olson & Dinerstein 2002). Globally, ca 97 percent of the remaining NDF is at risk and, and in Mesoamerica only about 5 percent is under some degree of protection against agricultural and ranching expansion (Miles et al. 2006). In this scenario of heavy fragmentation and defaunation (Melo et al. 2010), endozoochory by cattle and the response to frequent anthropogenic fire are two ecological factors that may play a crucial role in driving seed germination, and ultimately recruitment, in many plant species (Mouissie et al. 2005, Otterstrom et al. 2006). Indeed, several NDF tree species retain ‘anachronic’ traits that allow endozoochory (Janzen & Martin 1982, Guimarães et al. 2008); cattle may act as an efficient dispersal vector whose digestive system can scarify the seed coats facilitating germination (Traveset 1998). In addition, fire has long been known as a trigger of germination; thanks to its ability to release seeds from dormancy (Keeley & Fotheringham 2000). However, there are no studies assessing the potential interaction between endozoochory and fire in NDF despite its importance from an ecological and a restoration point of view.

Endozoochory and fire influence tree regeneration in different ways. First, fire acts on seeds once they have been dispersed, whereas the effects of endozoochory (i.e., seed scarification during gut passage) may start from frugivores' preferences. In fact, fruit traits such as size, shape, number of seeds per fruit and chemical composition may result in specific preferences by frugivores (Traveset 1998, Kitamura et al. 2002) that may affect the number of visits or the number of seeds dispersed per visit (i.e., the quantitative component of their effectiveness as seed dispersal agents, see Schupp 1993, Schupp et al. 2010). Thus, foraging choices can favor some species and have consequences on forest regeneration patterns at a landscape level (Eycott et al. 2007). Despite the knowledge of cattle preferences for the foliage of several NDF tree species (see Sandoval-Castro et al. 2005), little is known about their fruit preferences. Furthermore, a particular animal species can have significantly different effects on germination (i.e., positive, neutral, or negative) after passage of seeds through the gut depending on a variety of seed traits such as seed coat thickness, shape, or size (Traveset 1998, Campos-Arceiz et al. 2012). In short, the same dispersal agent can influence different species in unique ways due to differences in fruit traits related to frugivore attraction (Lomáscolo & Schaefer 2010), the number of seeds consumed per visit (Schupp et al. 2010), or differences in seed traits related to gut passage (Gardener et al. 1993, Benítez-Malvido et al. 2003, Venier et al. 2012). Nevertheless, few studies have addressed how these three stages of endozoochory (preference by frugivores, number of seeds consumed, and gut passage resistance) are related.

A second important difference is in the evolutionary time during which plants have been subjected to fire and seed consumption by cattle. While cattle may be a surrogate of the extinct Pleistocene megaherbivores which were present during several million of years (Janzen & Martin 1982, Guimarães et al. 2008), the effects of fire on the overall functioning and geographic distribution of NDF are not well understood. While the notion that fire has not been a natural and frequent disturbance prevails (Murphy & Lugo 1986, Vieira & Scariot 2006), we now know that in NDF human-induced fire has been pervasive over the last century (Miles et al. 2006, Griscom & Ashton 2011, Peguero & Espelta 2011) and has been present for several millennia (Denevan 1992, Dull 2004, Cooke 2005, Avnery et al. 2011). Although fire is widely known as a germination trigger, there are few studies addressing this topic in NDF tree species (Otterstrom et al. 2006). Moreover, although both endozoochory and fire have been reported to induce germination by means of coat scarification (Traveset 1998, Baskin & Baskin 2000, Keeley & Fotheringham 2000, Traveset et al. 2008), the interaction between them has not been explored. If germination patterns depend on the amount seed coats are scarified (Traveset et al. 2008), then will a seed that survives gut passage be positively, negatively or neutrally affected by the subsequent heat-shock effect of a fire? A positive interaction of these two factors would suggest that a more recent ecological factor (fire) is reinforcing the role of a long-term adaptation (endozoochory), while a negative interaction would suggest that fire is counterbalancing the benefits of endozoochory. Alternatively, if endozoochory has no effect on seed germination but fire does, this would suggest that cattle act only as seed dispersal vectors.

The aim of this study was to analyze the interaction between endozoochory and fire with three common Mesoamerican NDF tree species (i.e., Guazuma ulmifolia L. Malvaceae, Enterolobium cyclocarpum Griseb. Fabaceae, and Acacia pennatula Benth. Fabaceae). These species share endozoochory and physical dormancy as dispersal and germination syndromes, but differ in other traits that may influence cattle preference and the number of seeds ingested per foraging event. The two objectives were: (1) to evaluate differences in cattle preferences and whether there is a relationship between these preferences and the number of seeds ingested; and (2) to assess if an interaction exists between gut passage and subsequent heat-shock by fire that influences germination. To address these objectives, we carried out feeding trials and a germination experiment in which we tested the effect of seed scarification resulting from gut passage, which was simulated following a standardized in vivo–in vitro procedure, and the subsequent effect of fire, estimated by heat-shocks differing in temperature and exposure time. The results obtained may provide further insight into the ecological role that endozoochory and fire play in the dynamics of NDF tree species and, ultimately, provide valuable and urgent clues as to how to manage these two factors in order to foster the regeneration of transformed NDF.

Methods

  1. Top of page
  2. AbstractResumen
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. Literature Cited
  9. Supporting Information

Study area and species

Miraflor-Moropotente is a mountainous plateau (800–1200 m asl) in NW Nicaragua. It is a partially protected landscape, i.e., silvo-pastoralism is allowed but some practices such as logging and fire are precluded. This area is characterized by a dry tropical climate; monthly temperatures range from 16 to 33 °C and 90 percent of the 830 mm mean annual precipitation falls in a 6-mo wet season (May–October). The 290 km2 of the area are a mosaic of wooded rangelands surrounded by secondary and remnant NDF patches (Tarrasón et al. 2010, Somarriba 2012). Prescribed fires to clear encroached areas and to favor grasses are theoretically banned in protected areas, but during the dry season they are common (G. Peguero personal observation). Forest patches are widely dominated by Acacia pennatula Benth. (Fabaceae). Guazuma ulmifolia Lam. (Malvaceae) and Enterolobium cyclocarpum Jacq. Griseb. (Fabaceae) usually regenerate in pastures and are classified as pasture colonists and/or early successional trees (Esquivel et al. 2008, Peguero et al. 2012). The three species present a megafaunal dispersal syndrome (Janzen & Martin 1982) and with the exception of white-tailed deer (Odocoileus virginianus), and the locally rare white-lipped and collared peccaries (Tayassu peccary and Pecari tajacu), they have no natural dispersers in the region. Their seeds have physical dormancy (Baskin & Baskin 2000) and share similar fruiting phenology. Once ripened at the beginning of the dry season, fruits are actively fed on by cattle. After gut passage, at least some seeds germinate immediately after the first rains of the next wet season (G. Peguero personal observation). However, they differ in other traits that may condition the preference of frugivores as well as the number of seeds consumed per foraging event. Acacia pennatula produces protein-rich indehiscent flat dry pods of an average weight of 4.5 g (±1.3 SD) with a mean of 11 (±3.4 SD) hard-coated seeds weighing 0.06–0.1 gr. Guazuma ulmifolia produces spheroidal nuts with a hard woody core and a sweet outer coat with an average weight of 2.6 g (±0.9 SD) and a mean of 51 (±13 SD) tiny seeds (0.004–0.01 g) per fruit. Finally, Enterolobium cyclocarpum fruits are rounded, dry indehiscent pods with an average weight of 22 g (±5.1 SD) and a mean of 11 very hard-coated seeds (±3.2 SD) of 0.8–1.1 g per fruit. These fruit trait data come from a sample of at least 50 fruits collected from five individuals from each species.

Feeding trials

In August 2009 in a ranch within Miraflor-Moropotente, we habituated seven 6-mo-old calves (Brown Swiss × Brahman) to feeding in individual troughs. This habituation process was based in 5 d of offering a grain-bran based concentrate ad libitum for 5 min at dawn. After this period, we started five consecutive days of preference trials that consisted of offering fruits of A. pennatula, G. ulmifolia, and E. cyclocarpum in separate amounts of 0.3 kg per species in an individual trough. For 5 min, which was enough time to observe the onset of a potential choice but not enough to observe any of the offerings exhausted, we recorded the number of bites of each kind of fruit and weighed the amounts not consumed. Prior to the trials, the calves were fasted overnight; all trials were done from 6.00 h to 7.00 h to ensure a high and equivalent feeding motivation. All individuals were naive with respect to the fruits offered and to avoid conditioned learning, the position of the fruits in the individual troughs was randomly changed every day.

Germination experiment

To assess the potential additive effects of endozoochory and fire on the germination response of the three species studied, we conducted an ex situ germination experiment in which we combined the experimental simulation of gut passage with different thermal shock treatments in a balanced factorial design. To simulate the effects of gut passage on the seeds, we developed a three-step—(1) rumen; (2) abomasum-duodenum; (3) intestine—in vivo–in vitro standardized procedure in the facilities of the Ruminants Research Group (at the Autonomous University of Barcelona, Spain) in July 2010 (see Gardener et al. 1993 for a similar procedure). Fruits from five individuals of each species were hand-harvested and manually dehisced to obtain their seeds. Once in the laboratory, the seeds of each species from different individuals were pooled and put into sealed nylon bags in separate groups (Ankom Technology, Fairport, NY, U.S.A) and then in the rumen of a cannulated cow. After 48 h of rumen suspension, the bags were placed in glass incubation bottles containing 2 l of 0.1 N HCl adjusted to pH 1.9 with 1 g/l of pepsin (P-7000; Sigma, St. Louis, MO, U.S.A) for 2 h with constant rotation at 39 °C in DaisyII incubators (Ankom Technology). After incubation, the bags were rinsed with tap water and put into incubation bottles containing 2 l of a pancreatin solution (0.5 N KH2PO4 buffer adjusted to pH 7.75, containing 50 ppm of thymol and 3 g/l of pancreatin, P-7545, Sigma) and incubated for 24 h with constant rotation at 39 °C (adapted from Gargallo et al. 2006). Finally, to reproduce the anaerobic intestinal environment, rectal feces samples from three different cows were collected in plastic bags saturated with CO2 and immediately placed in a water-bath with a buffer solution of salt minerals (NaCl, KCl, NaPO4, KPO4) at 39 °C. The feces were manually crumbled in order to re-suspend fiber-associated bacteria and the solution was filtered through a 250 μm mesh screen and completed with a buffer solution of salt minerals until reaching a dilution of 0.2 g fecal sample per ml of buffer (adapted from Bindelle et al. 2007). The bags with the intestinal bacterial inoculum were incubated 24 h more with constant rotation at 39 °C in anaerobic conditions. Although it must be noted that retention times within a ruminant may vary depending on the size and specific gravities of the particles (i.e., seeds; Murphy et al. 1989), the incubation times applied followed those suggested by Warner (1981) and applied by Gardener et al. (1993) with which these latter authors did not find differences compared with natural passage rates of seeds in cattle.

Once the simulation of gut passage was done, we reproduced the effects of a pasture fire by exposing sets of seeds after ‘gut passage’ and without ‘gut passage’ (i.e., dispersed by endozoochory vs. non-dispersed) to different thermal shocks differing in temperature (60, 90, and 120 °C, as well as a ‘no heat-shock group’ hereafter referred to as ‘control’) and with two exposure times (2 & 6 min) using an electric heater. According to Gashaw and Michelsen (2002), this range of temperature and exposure time reliably reproduces the conditions of the upper soil layers or soil surface during fires in tropical grasslands. After all the ‘pre-germination’ treatments were applied (2 levels of ‘gut passage’ × 4 temperatures × 2 exposure times = 16 treatments), we set ten seeds of each species in 8.5 cm Petri dishes with moistened filter paper obtaining ten replicates (i.e., 1 Petri dish) per treatment. All dishes were set in a germination chamber with a constant environment of 21 °C, 70 percent RH and 300 μmol photons/m2 s in 16/8 h of light/dark photoperiod. All dishes were kept moistened with distilled water and germination (i.e., radicle protrusion) was recorded daily. The germinative response of all treatments leveled-off between the tenth to the twelfth day and there were no changes afterward (Figs S1 and S2). We therefore took as the final point of our survey, the fourteenth measure (see Gardener et al. 1993 for a similar methodology and exactly the same germination period). While the stabilization of the germination response does not mean that non-germinated seeds are no longer viable, our aim was not to assess the potential for the build up of a seed soil bank but rather to investigate the interaction between endozoochory and fire as triggers of germination.

Data analysis

Cattle fruit preference was assessed as differences in the number of bites taken of each kind of fruit and differences in the total fruit intake (grams ingested) of each plant species. In addition, we estimated the number of ingested seeds from the total fruit intake of each species through the species-specific ratio of seed number per gram of fruit. Although fruit intake and number of ingested seeds were not formally count variables, they largely depended on the number of bites given so they equally fitted a negative binomial distribution. Therefore, to deal with non-normality and over-dispersion of data in these three variables we performed negative binomial regressions using the GLIMMIX procedure with SAS software (SAS Institute Inc., Cary, NC, U.S.A) including fruit (3 plant species) as a fixed factor and day (5 consecutive days of feeding trials) as a continuous variable. To control the autocorrelation between the repeated measures carried out on the same calves (7 individuals), these were included as a residual random factor with an autoregressive covariance structure since the measures were evenly spaced in time (SAS 2009). The final differences in the proportions of germinated seeds per treatment were assessed by means of a generalized linear model with a binomial error distribution with untransformed data (Warton & Hui 2011) using the GLIMMIX procedure with SAS software (SAS Institute). In this analysis, plant species, gut passage, temperature and exposure time along with their interactions were included as fixed factors and the minimum adequate model was selected according to the lower AIC.

Results

  1. Top of page
  2. AbstractResumen
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. Literature Cited
  9. Supporting Information

The fruits of the three species tested were avidly eaten by all calves in all feeding trials. However, the significant differences observed on the number of bites taken as well as on the fruit intake per trial (respectively, F2, 12 = 6.67; P = 0.0113 and F2, 12 = 7.26; P = 0.0086) suggested fruits of G. ulmifolia and E. cyclocarpum were preferred over those of A. pennatula (Fig. 1A and B). Additionally, the differences in the ratio of seeds per gram of fruit among species led to strong differences in the mean number of seeds ingested by a calf in a single foraging trial (F2, 12 = 35.6; P < 0.0001). This was especially striking in G. ulmifolia, which has large numbers of tiny seeds packed into small fruits, but is also why the initial differences in fruit intake between E. cyclocarpum and A. pennatula resulted in similar numbers of seed ingested (Fig. 1C). Although there was significant individual-level variation in the number of bites, in the total fruit intake and consequently, in the number of ingested seeds (respective covariance parameters: 0.7809 ± 0.1183; 1.0117 ± 0.1467; 3.2553 ± 1.3269), these response variables did not change over the consecutive feeding trials (day, F1, 95 = 0.16; P = 0.6892 and F1, 95 = 0.00; P = 0.9950 F1, 95 = 0.00; P = 0.9982).

image

Figure 1. Fruit preferences and seed ingestion by cattle assessed by means of feeding trials: (a) No. of bites, (b) Fruit intake (gr), and (c) No. of ingested seeds. Values are means ± 1 SE. Different letters show significant differences according to Least Square means tests.

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There were no differences in our experiment between A. pennatula, G. ulmifolia, and E. cyclocarpum in the final germination percentages (species, F2, 406 = 0.92; P = 0.3991). However, heat-shocks consistently triggered germination of the three species tested, with higher germination percentages as heat-shock temperature increased (temperature, F3, 406 = 5.41; P = 0.0012; Fig. 2). Furthermore, the duration of the heat-shock had a significant effect: six minutes of exposure produced a four-fold germination increase (exposure time, F3, 406 = 5.41; P = 0.0012; respectively 10.2 ± 3 vs. 2.7 ± 1, mean ± SE significant differences according to the LS Means tests). By contrast, gut passage did not have a significant effect on germination (gut passage, F1, 406 = 2.57; P = 0.1097) and although it reduced the germination percentage of A. pennatula and E. cyclocarpum by 5–15 percent, these species-specific differences had only marginal significance (species × gut passage, F2, 406 = 2.64; P = 0.0727). Additionally, gut passage did not modify seed response either to heat-shock temperature (gut passage × temperature, F3, 406 = 0.66; P = 0.5766) or to exposure time (gut passage × exposure time, F1, 406 = 0.1; P = 0.7538), thus rejecting the potential positive or negative interaction between gut passage (endozoochory) and heat-shock (fire).

image

Figure 2. Effect of heat-shock temperatures on seed germination of Acacia pennatula, Guazuma ulmifolia, and Enterolobium cyclocarpum. Values are means ± 1SE. Different letters show significant differences among treatments differing in heat-shock temperature according to Least Square means tests.

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Discussion

  1. Top of page
  2. AbstractResumen
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. Literature Cited
  9. Supporting Information

Fruit preference

The results of our feeding trials indicate cattle are surrogate seed dispersal agents for many NDF tree species (Janzen & Martin 1982) and that they could be essential for the eventual regeneration of forests using passive strategies (Mouissie et al. 2005, Griscom & Ashton 2011, Holl & Aide 2011). Due to the great levels of defaunation that typically occur in the heavily fragmented NDF (Melo et al. 2010), including the Miraflor-Moropotente area, cattle are the main seed dispersal agent for several animal-dispersed tree species into pastures (see Miceli-Méndez et al. 2008 for an example in a similar system). The number of foraging visits and the number of seeds dispersed per visit (Schupp 1993, Schupp et al. 2010) can be of special relevance for forest regeneration at a landscape level (Eycott et al. 2007); our results suggest that many tiny seeds packed into easily edible small fruits lead to greater dispersal efficiency in terms of higher potential seed loads per foraging event (Fig. 1C). On the other hand, it is widely known that species with larger seeds tend to maintain larger reserves in storage cotyledons (Green & Juniper 2004) and are thus more likely to resist drought conditions (Leishman & Westoby 1994) and resprout after damage (Harms & Dalling 1997, Green & Juniper 2004). Hence, their hypothetical numerical disadvantage might be partially counterbalanced by their higher survival in high-stress or nutrient-poor conditions (Muller-Landau 2010). This potential colonization-related trade-off between fecundity, seed size, seed dispersal, and seedling tolerance merits further field research (Muller-Landau 2010).

Endozoochory and fire: two consecutive events fostering seedling establishment

Our results indicate that the seeds of the species tested can remain viable following gut passage. Though some authors have found that gut passage may have strong positive or negative outcomes on germination (Lewis 1987, Chapman et al. 1992, see also the review by Traveset 1998), our results support the hypothesis that the adaptive significance of large mammals to trees with endozoochory traits is exclusively linked with dispersal rather than scarification of seeds to trigger germination after dunging (Janzen 1981, 1982, Janzen et al. 1985). By resisting scarification during gut passage so as not to germinate immediately after dunging—likely to occur in the middle of the dry season—the passed seeds are those that become incorporated into the seed bank as the dung decomposes (Janzen et al. 1985, Baskin & Baskin 2000).

Our experiment suggests fire breaks seed dormancy of the three species tested. The effect of fire, estimated with heat-shocks in a range simulating low intensity pasture fires (Gashaw & Michelsen 2002), has consistently been shown to promote germination (Fig. 2). This fire-induced dormancy release may have special relevance in seasonal NDF, where the selection of early germination at the onset of the rainy season appears favored (Garwood 1983). Despite the fact that heat-shock triggered germination is known to exist in a variety of species with physical dormancy (Keeley & Fotheringham 2000), including several African and Australian Acacia sp. (Hanna 1984, Sabiiti & Wein 1987, Bradstock & Auld 1995, Mbalo & Witkowski 1997), this result has not been demonstrated in Neotropical trees. The ability to germinate after a pasture fire may help to explain the colonizing success of the species tested (for G. ulmifolia and E. cyclocarpum see Esquivel et al. 2008, Ribeiro et al. 2012, and for A. pennatula see Peguero & Espelta 2011), and may be extended to other NDF tree species with physical dormancy.

Finally, in light of the lack of additive effects of fire and gut passage scarification it appeared that breaking physical dormancy may be an all-or-nothing response rather than a function of the level of seed scarification (Traveset et al. 2008). In fact, heat-induced dormancy breakdown is usually based initially on the rupture of the strophiole cells, which may occur from a certain temperature threshold (Hanna 1984, Serrato-Valenti et al. 1995). Nevertheless, the remarkable variation in germination percentages observed here coincides with other structural and histochemical studies stressing that physical dormancy release is a more complex process than previously thought (Serrato-Valenti et al. 1995, Morrison et al. 1998). Moreover, considering that the use of experimental surrogates for endozoochory and fire may not capture the whole variability in these processes, the results presented here should be tested in more complex field situations and with additional species of conservation or restoration value.

Physical dormancy in NDF species: adaptation to endozoochory and exaptation to fire?

Recently Bradshaw et al. (2011) pointed out that physical dormancy may display selective advantages in highly seasonal environments where episodic seedling recruitment is favored. However, physical dormancy has multiple phylogenetic origins—it is present in 16 families—and it is not restricted to fire-prone ecosystems. Consequently, they conclude that this trait should be viewed as an exaptation to fire (Bradshaw et al. 2011). As such, physical dormancy in the species present in this study could have been selected to allow endozoochory by those large mammals with which these species interacted during several millions of years before their Pleistocene extinction (Janzen & Martin 1982). Moreover, physical dormancy is likely to have evolved precisely during this Miocene–Eocene period (Bradshaw et al. 2011). Notwithstanding this, anthropogenic fires may also drive the rapid evolution of seed traits such as seed coat thickness (Gómez-González et al. 2011) and despite the uncertainty regarding natural fire regimes in NDF before human settlement, it is now clear that anthropogenic fires have occurred for millennia and promoted a shift toward a more open landscape (Denevan 1992, Dull 2004, Avnery et al. 2011, Montoya & Rull 2011). Hence, although the origin of physical dormancy could be related to allow endozoochory, it is also likely that anthropogenic fire has played an important role favoring the maintenance of this trait as an exaptation despite the absence of seed dispersal vectors.

Conclusions

  1. Top of page
  2. AbstractResumen
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. Literature Cited
  9. Supporting Information

Our results suggest that the colonizing success of some NDF tree species may in part be due to dispersal by cattle, seeds resistant to gut passage, and pasture fires that break their physical dormancy such that their germination is concurrent with the onset of the rainy season. If NDF regeneration in pastures is to be fostered, a lack of seed dispersal can be overcome by taking advantage of cattle whose diet could be easily enriched with the fruits of those species retaining megafaunal dispersal traits (e.g., Cassia grandis, Albizia saman, Psidium guajava, Byrsonima crassifolia, Annona sp., Crescentia sp.). Afterward, targeted low intensity fires could be used to enhance germination and seedling establishment. Although the tree species studied are usually of low conservation concern, once established they can function as perching sites for birds and bats and provide shelter for other animal-dispersed trees, thus promoting forest regeneration (Holl et al. 2001). However, overgrazing, unsustainable stocking rates, and the indiscriminate use of fire must also be prevented, since they can also have an impact on the natural regeneration of forest species (Esquivel et al. 2008). Doing so will result in greater tree diversity and forest cover within pastures, which will not only increase the conservation value of anthropogenic landscapes (Chazdon et al. 2011) but also the economic benefits they provide (Harvey & Haber 1998, Harvey et al. 2008).

Acknowledgments

  1. Top of page
  2. AbstractResumen
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. Literature Cited
  9. Supporting Information

The authors thank Oscar R. Lanuza (Facultad Regional Multidisciplinaria, UNAN-Managua) for his valuable help with feeding trials, and Jordi Bartolomé, Sara Cavini and Maria Rodríguez of the Ruminants Research Group (UAB) for their assistance during the germination experiment. Albert Vilà and Oriol Lapiedra provided useful statistical comments. Susan Rutherford kindly edited English and the editors along with three anonymous reviewers greatly improved the manuscript with their constructive revisions. This research was funded by project D/026276/09 of the Spanish Agency for International Cooperation and Development (AECID). G. Peguero was supported by an FI grant from the Generalitat de Catalunya.

Literature Cited

  1. Top of page
  2. AbstractResumen
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. Literature Cited
  9. Supporting Information
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Supporting Information

  1. Top of page
  2. AbstractResumen
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. Literature Cited
  9. Supporting Information
FilenameFormatSizeDescription
btp12076-sup-0001-FigS1-S2.docxWord document82K

FIGURE S1. Germination-time response curves of the three species tested.

FIGURE S2. Germination-time differences among heat-shock treatments.

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