Seed Predation by Rodents Results in Directed Dispersal of Viable Seed Fragments of an Endangered Desert Shrub 1,2, 1,2,3 1,2,3 ANDREA P

Seed predation by rodents results in directed dispersal of viable seed fragments of an endangered desert shrub 1,2, 1,2,3 1,2,3 ANDREA P. L OAYZA, DANNY E. CARVAJAL, PATRICIO GARCI´A-GUZMA´ N, 1,3,4 1,3,4 JULIO R. GUTIERREZ, AND FRANCISCO A. SQUEO

1Departamento de Biologıá, Facultad de Ciencias, Universidad de La Serena, Benavente 980, La Serena 1720170 Chile 2Instituto de Ecologıá y Biodiversidad, Casilla 554, La Serena, Chile 3Programa de Doctorado en Biologıá y Ecologıá Aplicada, Universidad de La Serena, La Serena, Chile 4Centro de Estudios Avanzados en Zonas A´ ridas, La Serena, Chile

Citation: Loayza, A. P., D. E. Carvajal, P. Garcı´a-Guzma´n, J. R. Gutierrez, and F. A. Squeo. 2014. Seed predation by rodents results in directed dispersal of viable seed fragments of an endangered desert shrub. Ecosphere 5(4):43. http://dx. doi.org/10.1890/ES13-00283.1

Abstract. Seed predation and seed dispersal are important ecological processes with antagonistic effects on plant recruitment. In the southern edge of the Atacama Desert in Chile, Myrcianthes coquimbensis is an endangered, large-seeded, vertebrate-dispersed shrub that in the present-day has no known dispersers. Native rodents hoard and eat the seeds of M. coquimbensis but leave viable seed fragments at the hoarding sites; soil interspaces within rock outcrops where seedlings recruit. Here we examined whether rodents act as effective dispersers of M. coquimbensis by discarding viable seed fragments in sites suitable for recruitment. We simulated different levels of endosperm loss to determine if seedlings could develop from seed fragments. We assessed how frequently rodents discarded fragments, and the probability that these fragments produced seedlings. Finally, we compared emergence and seedling survival at the hoarding sites and in two other habitats where seeds arrive to evaluate the suitability of the hoarding sites. Seeds of M. coquimbensis developed seedlings even after 87% of their storage tissue was removed. Rodents left seed fragments in more than 50% of the trials; almost 60% of the discarded fragments produced seedlings. Seedlings did not emerge from open ground habitats, and emergence was higher under M. coquimbensis shrubs than in rock habitats. Survival of two-year-old seedlings was higher in rock habitats than under conspecific adult shrubs. Our results suggest that rodents may play a dual role in the recruitment dynamics of M. coquimbensis, acting simultaneously as seed predators and effective dispersers. Therefore, though seed predators impose costs, their net effect on plant fitness in this system—where dispersers of large- seeded species have been lost—is likely positive.

Key words: anachronism; Atacama; captive feeding trials; hoarding; Myrcianthes coquimbensis; rodent; seedling establishment.

Received 13 September 2013; revised 15 November 2013; accepted 19 November 2013; final version received 12 March 2014; published 8 April 2014. Corresponding Editor: R. Parmenter. Copyright: Ó 2014 Loayza et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/3.0/ E-mail: [email protected]

INTRODUCTION leads to a reduction of seed densities, and can limit plant recruitment and abundance (e.g., Seed predation and seed dispersal are impor- Orrock et al. 2006, Ferreira et al. 2011, Bricker tant ecological processes with antagonistic effects and Maron 2012). Conversely, seed dispersal is a on plant population dynamics. Seed predation process that can increase seed survival and,

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Fig. 1. A G. vibrunoides seedling emerging from a discarded seed fragment. ultimately promote plant establishment (e.g., 2011, Shiels and Drake 2011). The fates of these Fragoso et al. 2003, Blendinger et al. 2011, Hirsch seed fragments has been rarely addressed in the et al. 2012). Therefore, the loss of dispersers can literature, but the empirical data available shows hinder the regeneration of plants that depend on that although partial consumption can result in them (Loayza and Knight 2010, Calvinõ-Cancela seed death or decreased seed survival (Vallejo- et al. 2012, Traveset et al. 2012) and may Marıń et al. 2006, Shiels and Drake 2011), eventually increase their chance of becoming discarded seed fragments can also germinate extinct (McConkey and Drake 2002, Babweteera and establish (e.g., Perea et al. 2011). Therefore, et al. 2007). effective seed dispersal by rodents may also Nonetheless, there are some examples of plant occur, even if the seed has been partially species with large-seeded fruits that have pre- consumed. sumably lost their dispersers, but have been able In the southern limit of the Atacama Desert, to persist without them (Janzen and Martin 1982, Myrcianthes coquimbensis is a fleshy-fruited, large- Guimara˜es et al. 2008). The mechanism proposed seeded species that has no present-day dispers- to explain the persistence of these species is that ers, but whose fruit traits strongly suggest seed dispersal by scatter-hoarding rodents may adaptations for vertebrate dispersal. Along its have substituted the services provided by the area of distribution, natural seedling recruitment original dispersers (Guimara˜es et al. 2008). of M. coquimbensis is extremely low (Garcıá- Scatter-hoarding rodents bury intact seeds in Guzmań et al. 2012), and limited to soil spaces shallow caches, and those seeds that are not found within large rock outcrops (rock habitats retrieved by the animals, are protected from hereon). Seeds, however, cannot reach these invertebrate predation, and can germinate and habitats unless dispersed there by an animal establish (Briggs et al. 2009, Hirsch et al. 2012, vector. Rodents usually hoard seeds to these Jansen et al. 2012). Thus, seed dispersal by habitats, and either gnaw and destroy them scatter-hoarding rodents results from forgotten completely, or eat part of the seed leaving cached or re-cached intact seeds. fragments of different sizes at the hoarding sites; Generally, however, rodents will not disperse they do not cache the seeds and few, if any, are intact or undamaged seeds; instead, they remove left intact at the sites (A. P. Loayza, D. E. Carvajal, the seeds and either (1) eat them completely or P. Garcıá-Guzmań, personal observations). None- (2) partially consume them, discarding uneaten theless, seedlings occasionally emerge from seed seed fragments (e.g., Steele et al. 1993, Perea et al. fragments (Fig. 1).

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Here we tested the hypothesis that by hoard- occupying a coastal strip of 83 km long by ing seeds of M. coquimbensis to rock habitats, approximately 1 km wide (Garcıá-Guzmań et al. rodents act as effective dispersers of this species 2012). M. coquimbensis flowers from October even after partially destroying the seed. To test through February, ripe fruits are available from this hypothesis we collected four sets of inde- late August through January, with the peak of the pendent empirical data. First, we evaluated fruiting season in October. Fruit production per whether seeds with large fractions of the endo- individual plant is highly variable, ranging from sperm removed could produce seedlings. Sec- ,10 to .1500 fruits. Ripe fruits are large (2.5 3 ond, we quantified how frequently rodents leave 3.5 cm), fleshy, red berries that generally contain seed fragments when feeding. Third, we planted only one seed (0.8–2.5 cm diameter, weighing on seed fragments discarded by rodents after average 2.6 g, but reaching up to 6 g), although a feeding to assess how often these fragments single fruit may occasionally have up to three produced seedlings. Finally, to determine if the seeds. Fruits possess a sugary water-rich pulp, rock habitats where rodents hoard the seeds and and have a low pericarp:seed mass ratio (0.38). leave the fragments are suitable sites for plant Seeds are monoembryonic and recalcitrant (i.e., recruitment, we (1) compared emergence in these they are large and photosynthetically active); habitats with those of two other habitats where they can germinate epigeally from fallen fruits seeds can arrive and, (2) followed and compared and do not persist in the soil seed bank for more the fate of naturally occurring seedlings of M. than a few weeks before drying out. Seedling coquimbensis for two years. emergence in the field depends on the amount of annual rainfall, but it is generally low and MATERIAL AND METHODS usually restricted to rock habitats. After emergence, there is extensive mortality due to Study area and species summer droughts. We conducted this study in the southern limit Three species of native rodents (Octogon degus, of the Atacama Desert, 26 km south of La Serena, Abrothrix olivaceus, and Phyllotis darwini) are seed 0 0 Chile (30804 S, 71814 W; 0–33 m.). The area is predators of M. coquimbensis. Octogon degus is a dominated by Eulychnia acida, Echinopsis coquim- diurnal, colonial and fossorial species (Woods bensis, Copiapoa coquimbana, Oxalis gigantea, Lith- and Boraker 1975) that is reported to use both raea caustica, Heliotropium stenophyllum, Fuchsia larder- and scatterhoarding to store seeds licyodes and Myrcianthes coquimbensis.Shrub (Quispe et al. 2009). Conversely, A. olivaceus canopies cover between 25-30% of the ground; and P. darwini are both nocturnal species, which the rest of which is devoid of plants, except after scatter-hoard seeds (Vasquez 1996). rains when annuals cover the desert floor. The landscape is also characterized by the presence of Emergence from seed fragments large granite rock outcrops (i.e., rock habitats); We simulated the effect of rodent predation on these outcrops and the crevices within them emergence by experimentally cutting portions of generate shady habitats where soil moisture (x¯ ¼ the seed’s storage tissue and comparing seedling 14.02%,SD¼ 7.64) is higher than in open habitats emergence among different cutting treatments. (x¯ ¼ 8.54%,SD¼ 6.50, t ¼3.8, df ¼ 93, P , 0.001) Specifically, we selected 80 seeds of approximate- (A. P. Loayza, unpublished data). Water in this ly the same size (x¯ ¼ 2.64, SD ¼ 0.53) and system comes from occasional rains, as well as randomly assigned each seed to one of four from coastal fogs. Mean annual temperature is cutting treatments: (1) intact seeds (no cutting); 14.28C; annual rainfall ranges from 21 to 122 mm (2) seeds cut in half; (3) seeds cut into four pieces (75 6 33, mean 6 SD), and falls predominantly or; (4) seeds cut into eight pieces. Before and after between June and August (CEAZAMET 2004– being cut, each seed was weighed individually in 2012). an analytical balance (Scaltec, SBA31) to calculate Myrcianthes coquimbensis (Barneóud) Landrum the percentage of storage tissue removed. Cut- and Grifo (Myrtaceae) is an endangered, ever- ting treatments resulted in a reduction of the green shrub, endemic to the Elqui Province in storage tissue by 31–46% for seeds cut in half, by Chile. It has an extremely narrow distribution, 64–79% for seeds cut in four, and by 85–87% for

v www.esajournals.org 3 April 2014 v Volume 5(4) v Article 43 LOAYZA ET AL. seeds cut into eight pieces. In each case we were processed by rodents, emergence was examined careful to leave one of the seed fragments with once a month for six months and the presence of the embryo intact; these fragments were sown in emerged seedlings recorded in each survey. plastic pots, watered twice a week and checked To test if survival of the early stages of M. for seedling emergence once a week for five coquimbensis differed between habitats, we mon- months (August–December). itored the fate of naturally occurring seedlings in permanent plots established in 2011. We estab- Rodent trials lished four permanent 25 m 3 25 m plots in each To determine if seed fragments discarded by of seven localities across the distribution range of native rodents could germinate and develop M. coquimbensis (Garcıá-Guzmań et al. 2012). seedlings, we captured rodents present at the Within each plot, all M. coquimbensis plants were study site and fed them M. coquimbensis seeds. In individually tagged, classified into stages, and November 2012 we conducted a trapping session the habitat where they were present was record- during two consecutive nights and days using a 5 ed. Seedling fate was followed for all marked 3 6 trapping grid (25-m station intervals), with seedlings once a year during two years. two Sherman-style aluminum folding live traps (30 cm 3 11 cm 3 9 cm; Sherman Traps, Statistical analyses Tallahassee, Florida, USA) per station (n ¼ 60). We examined whether experimental removal Each trap was baited with rolled oats and of the storage tissue affected seedling emergence checked before sunrise and before sunset. We using generalized linear models with Poisson recorded sex, reproductive condition, and body error distributions. We considered cutting treat- mass of each captured individual, and brought ment as the main factor, and number of emerged them into the laboratory. Each individual was seedlings as the response variable; significance then caged singly and provided with water, was tested using a chi-square likelihood ratio rolled oats, and four whole M. coquimbensis test. Additionally, we evaluated if the removal of seeds. At the end of the day or night (depending seed storage tissue affected temporal patterns of when the individual was fed), we checked the seedling emergence with Kaplan-Meir survival cages to see if seeds had been eaten. When seeds analysis, where the fraction of emerged seedlings were eaten, all the remaining fragments (with or in each cutting treatment is analyzed as a without an embryo) were collected and sown function of time. We assessed whether the individually in plastic pots. Pots were watered proportion of emerged seedlings from discarded twice a week and emergence was checked once a fragments differed among rodent species with a week for four months (November–February). All chi-square. We used generalized linear models, individuals were returned to their capture site with quasi-Poisson (for the 2011 data) or Poisson after the feeding trial ended. (for the 2012 data) error distributions to determine if the probability of seedling emergence Seedling emergence and survival differed among habitats. For both years, habitat During the peak of the fruiting seasons of 2011 was the main factor, and number of emerged and 2012, we sowed a group of 10 seeds in each seedlings the response variable. We examined of three habitats: (1) rock habitats (where rodent habitat-specific differences in survival of natural- hoards are found); (2) under adult M. coquimben- ly occurring seedlings in the field with a sis shrubs (where the majority of fruits fall); and proportions test. Finally, we explored early (3) open ground (where fruits can occasionally recruitment dynamics of M. coquimbensis by arrive by rolling down slopes). Seeds were estimating habitat-specific transition probabili- extracted manually from ripe fruits, and since ties (TPs), calculated as the mean number of they are not regularly buried, they were only individuals completing a stage divided by the partially covered with a thin layer of soil (,0.5 number of individuals entering that stage (Rey cm). Each habitat was replicated 10 times, and in and Alcańtara 2000). We then calculated the each replicate seeds were protected from preda- cumulative probability of early recruitment for tors with 25 3 15 3 10 cm wire cages with a mesh each habitat as the product of the individual TPs. size of ca. 1 cm2. To mimic the fate of seeds All statistical analyses were conducted using the

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Fig. 2. Proportion of emerged seedlings under adult M. coquimbensis shrubs and in soil spaces of rock outcrops for 2011 and 2012. Error bars indicate 61 SE.

R statistical environment, version 3.1.1 (R Devel- emerged in 2011; in contrast in 2012, emergence opment Core Team 2013). reached 30%. No seedlings emerged from open ground sites on either year, thus we excluded this RESULTS habitat from statistical analyses. Probability of emergence for both 2011 (v2 ¼ 4.86, df ¼ 18, P ¼ Cutting treatment had no effect on either the 0.05) and 2012 (v2 ¼ 4.86, df ¼ 18, P ¼ 0.03) was number of seedlings emerged (v2 ¼ 0.49, df ¼ 78, higher under adult M. coquimbensis shrubs than P ¼ 0.48) or the temporal pattern of seedling in soil spaces of rock outcrops (Fig. 2). emergence (v2 ¼ 2.00, df ¼ 3, P ¼ 0.57). Natural recruitment of M. coquimbensis in the Consequently, M. coquimbensis seedlings are able field is extremely low. In 2011, only 20 of ca. 1200 to emerge from seed fragments that are up to plants marked within the permanent plots were 87% smaller than the original seed, as long as the seedlings (,0.02% of the population). Of these embryo is unharmed. seedlings, nine were under shrubs and 11 in rock We captured a total of 24 individuals of the habitats; no seedlings were recorded in open three rodent species: Octogon degus (n ¼ 1), ground sites. The proportion of seedlings that Abrothrix olivaceus (n ¼ 13), and Phyllotis darwini survived to one-year saplings did not differ (n ¼ 10). On average, A. olivaceus and P. darwini between rock habitats and under M. coquimbensis left seed fragments on ca. 70% of the trials, which shrubs (Z ¼1.82, P ¼ 0.07). However, the suggests that these species commonly discard proportion of seedlings that survived to two-year some portions of a seed. Of 54 seed fragments saplings was higher in rock habitats than under collected from A. olivaceus and P. darwini during adult M. coquimbensis shrubs (Z ¼3.30, P , the experiment, 59% (n ¼ 32) developed a 0.001); in fact, no seedlings survived after one seedling; there were no differences in the year under conspecific plants. Thus, our results proportion of seedlings produced by seed frag- suggest that although emergence is higher under ments discarded by either species (v2 ¼0.02, df M. coquimbensis, recruitment is ultimately limited ¼ 1, P ¼ 0.89). In the feeding trial with the only to rock habitats (Table 1). individual captured of O. degus, we collected three seed remnants; of those two produced a DISCUSSION seedling. Only 4% of the seeds sown in the field We show that rodents are effective dispersers

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Table 1. Habitat-specific transition probabilities of M. coquimbensis seeds and seedlings for 2011 and 2012. CPR, cumulative probability of early recruitment.

Habitat Transition Under M. coquimbensis plants Soil spaces in rock outcrops Seed to first-year seedling 0.360 0.165 First-year seedling to third-year sapling 0.000 0.636 CPR ... 0.105 of M. coquimbensis seeds, even after partially produce a seedling. For example, among the destroying them. By discarding viable seed Myrtaceae, Teixeira and Barbedo (2012) showed fragments at the hoarding sites, rodents are that seed fragments of several species of Eugenia effectively transporting embryos to suitable sites (E. brasiliensis, E. cerasiflora, E. involucrata, E. for recruitment. Because M. coquimbensis has no pyriformis,andE. uniflora) could produce a present-day dispersers, rodents are acting as seedling whether or not they had the embryo, substitute dispersers of this endangered plant. which indicates the presence of meristematic However, unlike other studies, in which effective tissues in the seeds capable of differentiating and seed dispersal by rodents is ultimately the result forming new embryos. Similarly, Joshi et al. of forgotten cached or re-cached intact seeds, our (2006) found that fragments of Garcinia gummi- results provide empirical evidence of a system gutta seeds, irrespective of their size, could where the almost complete destruction of a seed produce both roots and shoots. Although, in via seed consumption can, nonetheless, result in our study we did not test explicitly whether effective dispersal. fragments of a single seed could produce Seeds of M. coquimbensis have the ability to different seedlings, we have anecdotal evidence develop roots and seedlings from seed fragments that suggests that M. coquimbensis may also have up to 87% smaller than the original seed. The this capability. If so, this would increase the ability to germinate from partially destroyed potential of seed fragments leftover by rodents at seeds has been reported for several large-seeded the hoarding sites to develop into seedlings. species (e.g., Dalling et al.1997, Joshi et al. 2006, The fruit traits of M. coquimbensis are strongly Vallejo-Marı´netal.2006,Pe´rez et al. 2008, indicative of vertebrate dispersal; this is consis- Teixeira and Barbedo 2012). This ability is likely tent with other Myrcyanthes species in the retained because larger seeds have greater Neotropics, which are dispersed by birds and/ quantities of nutritional tissue, which allows or monkeys (Barberis et al. 2002, Pizo 2002, them to withstand different levels of endosperm Wilms and Kappelle 2006). However, as men- loss (Dalling et al. 1997, Mack 1998). If so, then it tioned previously there are no present-day is possible that the majority of M. coquimbensis dispersers of M. coquimbensis. Along its range, seeds that germinate after being partly con- some species of birds (e.g., Mimus tenca, Turdus sumed, are those in the larger size range. If seed sp.) peck the pulp of ripe M. coquimbensis fruits size is heritable, this could eventually result in a that are still attached to the plant, but none are shift towards shrubs producing larger seeds. large enough to either carry a fruit or swallow a In our study, we did not quantify the percent- seed. It is possible then, that the animals that age of discarded fragments in which the embryo originally dispersed its seeds are no longer was unharmed; therefore, we assume that frag- present. Whether M. coquimbensis represents an ments that produced seedlings were those where anachronic dispersal system is unknown, but the damage was located in non-embryonic tissue. there is ample archeological evidence of fauna Avoidance of the seed parts that contain the that went extinct in the area towards the end of embryo has been found in other studies (e.g., the Pleistocene (Moreno et al. 1994, Borrero 2009, Perea et al. 2011), and may be related to higher Jackson et al. 2011) that may have consumed the tannin contents in these parts (Steele et al. 1998). fruits of M. coquimbensis. For example, there are The presence of the embryo, however, is not fossil records of several herbivores (e.g., Cuvier- always a requirement for a seed fragment to onius, Megatherium, Macrauchenia, among others),

v www.esajournals.org 6 April 2014 v Volume 5(4) v Article 43 LOAYZA ET AL. which have been recognized as potential dispers- that rodents play a dual role in the recruitment ers of other extant large-seeded species (Janzen dynamics of M. coquimbensis, acting simulta- and Martin 1982). neously as seed predators and effective dispers- Emergence and seedling survival of M. coquim- ers of predated seeds. The relative importance of bensis in the field is very low and contingent not each role, however, will probably depend on the only on the amount of rainfall, but also on the environmental context. For example, although habitat. In our study, emergence was higher rodents discarded fragments in ca. 70% of the under adult conspecific shrubs than in rock feeding trials, in the field in years of low fruit habitats. This could be because the soil under- production (and consequently lower seed avail- neath M. coquimbensis shrubs accumulates large ability), rodents are unlikely to satiate and may quantities of leaf litter, which can influence discard fragments less frequently, if at all. germination cues, such as moisture and temper- Conversely, seed fragments may be discarded ature (Carson and Peterson 1990), as well as more frequently when fruit and seed abundances release leachates that can be a source of mineral are high. To fully discern the role of rodents on nutrients (Facelli and Pickett 1991). Moreover, the recruitment of M. coquimbensis, this hypoth- the presence of leaf litter can be important to esis needs to be tested. maintain soil moisture when rainfall is low, Finally, though seed predators certainly im- particularly for species with recalcitrant seeds pose costs, their net effect on plant fitness in this that cannot form a seed bank (Becerra et al. system, where the dispersers are absent, is not 2004). However, the spatial pattern of initial necessarily negative. Our results highlight that recruitment was not maintained through later the costs and benefits of an animal-plant interac- plant stages, as seedlings did not survive tion are not always evident (Shiels and Drake underneath conspecific shrubs. Although leaf 2011, Arnan et al. 2012), and in our case a litter may also negatively impact seedling sur- predominantly antagonistic interaction between vival (Facelli and Pickett 1991), all of the rodents and M. coquimbensis seeds, may be seedlings that were marked under adult M. considered a mutualism in the sense that rodents coquimbensis shrubs eventually dried out, which are currently the only vertebrates that effectively suggests that competition for water with the promote recruitment of M. coquimbensis. adult conspecific was the most likely cause of mortality. In contrast, seedlings survived more in ACKNOWLEDGMENTS rock habitats, probably because soils in these habitats retain moisture for several months after I thank all those who assisted with the field data the winter rains (A. P. Loayza, unpublished data), collection, particularly Hernań Vasquez and Paloma allowing seedlings the time to develop deeper Gachoń. Comments from Rodrigo Rios and Cristina root systems. Given that our data on seedling Armas helped improve an earlier version of the manuscript. This research was supported by grants survival come from only 20 naturally occurring awarded to A. P. Loayza from the Rufford Small Grant seedlings in the field, we cannot conclude with Foundation and a FONDECYT Post-Doctoral Research certainty that rock habitats are always better Grant (3120123). J. R. Gutierrez was supported by a recruitment sites for M. coquimbensis as survival FONDECYT grant (11102128). P. Garcıá-Guzmań was may be context-dependent. Nonetheless, because supported by a CONYCIT doctoral fellowship almost 70% of all of the plants marked across the (21120854). Statement of authorship: A. P. Loayza distribution range of the species are associated to collected data, performed statistical analyses and rock habitats, it is feasible that recruitment is wrote the first draft of the manuscript. D. E. Carvajal strongly limited to these habitats. and P. Garcıá-Guzmań collected data and contributed substantially to revisions. J. R. Gutierrez and F. A. The role of rodents as both seed predators and Squeo contributed substantially to revisions. dispersers remains largely unexplored. Partial consumption of seeds may have important LITERATURE CITED consequences on plant community structure and population dynamics in several systems Arnan, X., R. Molowny-Horas, R. Rodrigo, and J. (e.g., Pearson and Theimer 2004, Perea et al. Retana. 2012. Uncoupling the effects of seed 2010, Shiels and Drake 2011). Our results show predation and seed dispersal by granivorous ants

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