Table Of ContentMadrono, Vol. 62, No. 1, pp. 21-32, 2015
DELAYED SEED DISPERSAL IN CALIFORNIA DESERTS
Alejandra MartInez-Berdeja*
Department of Botany and Plant Sciences, University of California, Riverside,
900 University Ave, 2140 Batchelor Hall, Riverside, CA 92521
^ [email protected]
Exequiel Ezcurra
Department of Botany and Plant Sciences, University of California, Riverside,
900 University Ave, 3324 Olmsted Hall, Riverside, CA 92521
Andrew C. Sanders
University of California, Riverside Plant Herbarium, University of California, Riverside,
900 University Ave, 2140 Batchelor Hall, Riverside, CA 92521
Abstract
Serotiny and delayed seed dispersal are thought to have evolved as traits allowing plants to cope
with environmental variability. We conducted a literature search of serotinous desert plants in the
Mojave and Sonoran deserts in California and classified them according to their seed retention
syndrome. Serotinous species in North American deserts have evolved similar seed retention
syndromes as those of plants in other deserts of the world. Seed retention in deserts plants is a
common seed dispersal strategy in arid ecosystems that allows plants to cope with environmental
variability and unpredictability.
Resumen
Se cree que la serotinia y la dispersion retrasada de semillas han evolucionado como un mecanismo
que permite a las plantas hacer frente a la variabilidad ambiental. En el presente estudio realizamos
una busqueda en la literatura sobre las plantas serotinas de zonas aridas en los desiertos del Mojave y
Sonorense en California. Las plantas encontradas fueron clasificadas de acuerdo al sindrome de
retencion de semillas. Las especies serotinas de los desiertos de Norte America han evolucionado
sindromes de retencion de semillas similares a los de las plantas de otros desiertos del mundo. La
retencion de semillas en plantas de desierto es una estrategia de dispersion comun en los ecosistemas
aridos que permite a las plantas adaptarse a la variabilidad e impredecibilidad ambiental.
Key Words: Basicarpy, delayed dispersal, desert serotiny, dispersal syndromes, hygrochasy, rain pulses.
Serotiny consists of the retention of mature also evolved in arid environments. In the central
seeds within the maternal canopy, delaying seed Namib Desert, around eleven species have been
dispersal for varying periods of time (also known shown to retain seeds (Giinster 1992). Similarly,
as bradychory or delayed dispersal; Lamont 1991; about 40 species in Israel and the Sinai have
Thanos 2000, 2004). Serotiny has been described in been described as having delayed dispersal
different pulse-driven ecosystems such as the mechanisms triggered by the onset of rains
seasonally dry, fire-prone mediterranean woody (Gutterman and Ginot 1994). Environmental
scrubs and temperate forests in Australia, South pulses in desert ecosystems—in the form of
Africa, and North America (Le Maitre 1985; randomly varying water availability—constitute
Lamont 1991; Lamont and Enright 2000). The a major factor driving the dynamics of desert
adaptive significance of seed retention and delayed communities (Noy-Meir 1973; Loik et al. 2004;
dispersal in these environments has been interpret¬ Reynolds et al. 2004). The serotinous retention
ed as providing protection to seeds from predators of seeds seems to be advantageous in environ¬
and bums (Enright et al. 1998a, b), synchronizing ments where conditions for successful germina¬
seed release in a nutrient rich environment and tion and establishment pulsate more or less
with decreased competition for light and water, randomly, and where the probability of estab¬
thus allowing for higher seedling establishment lishment outside an ephemeral pulse period is
(Lamont 1991), and reducing post-dispersal haz¬ relatively low.
ards by swamping the predator populations with The objective of this paper is to provide a list
high number of seeds (Janzen 1976). of serotinous species in the Mojave and northern
Despite the fact that most of the literature on Sonoran Desert in the flora of California. We
serotiny gravitates around fire-driven ecosys¬ also classify seed retaining species according to
tems, seed retention and delayed dispersal have their different seed retention syndromes.
22 MADRONO [Vol. 62
Methods Table 1. Order, Family, and Genera of Desert
Species in the Mojave and Sonoran Deserts.
We did a literature search in two regional
desert floras: Flora of the Gran Desierto and Rio Serotinous
Colorado of Northwestern Mexico (Felger 2000) Order Family Genera species
and The Jepson Desert Manual: vascular plants of Asparagales Agavaceae 1 1
southeastern California (Baldwin et al. 2002). Caryophyllales Amaranthaceae 2 1
Although Felger’s flora deals with Mexico’s Gran Asterales Asteraceae 121 1
Desierto and not strictly with Californian deserts, Boraginales Boraginaceae 11 1
Caryophyllales Cactaceae 8 4
the region is a natural continuation of the Lower
Celastrales Celastraceae 1 1
Colorado Valley across the Mexican border, and
Mai vales Malvaceae 9 2
the book contains very valuable descriptions of
Myrtales Onagraceae 6 3
plants common to the larger desert region. In Lamiales Orobanchaceae 1 1
both books we looked for indications of serotiny Poales Poaceae 74 2
in botanical descriptions such as “dry dead Caryophyllales Polygonaceae 13 1
skeletons remain on the field for several years Sapindales Simaroubaceae 1 1
retaining seeds”, or for terms associated with seed Solanales Solanaceae 8 2
Zygophyllales Zygophyllaceae 5 1
retention, such as “tardily or irregularly dehiscent
Total 261 22
fruit”, “woody persistent fruits”, and “indehis-
cent fruit” among others.
We narrowed this broad first list by eliminating
3.7% of those listed in the Flora of the Gran
species that, although having lignified structures,
Desierto (Felger 2002). This estimate represents a
readily release their seeds at the end of the
minimum threshold, as other serotinous species
growing season. We did this based on our own
may exist that have not been identified with the
field notes and by consulting with experts on the
procedure we followed. The ability to retain seeds
flora of the regional deserts. We then verified our
seems to be taxonomically widespread: 14 out of
results through a more in-depth literature search,
114 families of desert plants (12.3%; two mono¬
looking for information on the dispersal charac¬
cot families and 12 dicot families) belonging to 13
teristics, life cycle, growth season, habitat, and
different orders have at least one serotinous
distribution of species with apparent seed reten¬
species (Table 1; a detailed list is provided in
tion syndromes in the Sonoran and Mojave
Appendix 1). After inspecting the range and type
deserts (references consulted are listed in the
of seed-retaining strategies we found, serotinous
following section). Finally, we confirmed our
species were classified into the following six
information using herbarium specimens (Univer¬
groups: (1) ground-level ephemerals, (2) persis¬
sity of California, Riverside Plant Herbarium
tent plants with lignified fruits, (3) gradually
[U CR]; http ://www. herbarium. ucr.edu/Herbarium.
opening capsules, (4) reproductive dimorphism,
html) and looked for evidence of prolonged seed
(5) schizocarps with heteromericarps, and (6)
retention on the specimens, to come with a list of
persistent fruits.
serotinous species in the California desert region.
Serotinous desert plants have been classified
1. Ground-level Ephemerals (basicarpy)
according to the period of time of seed retention
(Zohary 1962; van der Fiji 1982; van Oudtshoorn
Basicarpic species are desert ephemeral plants
and van Rooyen 1999). However, because of the
that produce flowers immediately above ground
lack of data on seed-retention times within the
level, and retain their seeds in hard, lignified
Sonoran and Mojave deserts, we classified our
structures for a long period of time after the
plants into two types: (a) strongly serotinous
mother-plant dies, releasing seeds to rainfall
species were identified as those that possess
events (Ellner and Shmida 1981). A basicarpic
tough, strongly lignified seed-retaining structures,
species in the California desert region is Chor-
and (b) weakly serotinous species were identified
izanthe rigida (Torr.) Torr. & A. Gray (Poly-
as those showing softer, or less rigid seed-
gonaceae), a short (2-15 cm) winter annual
retaining structures (suggesting that seed reten¬
whose dead, spiny skeletons persist for several
tion occurs for a shorter time period). years releasing involucres to rainfall events
(Fig. la; Felger 2000; Baldwin et al. 2002).
Results Chorizanthe rigida is associated with desert
pavements (Martinez-Berdeja et al. 2013), and is
In total, we identified 21 strongly serotinous distributed from the Great Basin to the Mojave,
and nine weakly serotinous species. Of the 30 Colorado, and northern Sonoran deserts. Al¬
serotinous species, 27 were dicots and only three though Ellner and Shmida (1981) classified this
were monocots. The plants we identified as seed- species as basicarpic, it is noteworthy that, while
retaining form 1.1% of the species listed in The the plant is low (ca. 5 cm) in the Mojave, towards
Jepson Desert Manual (Baldwin et al. 2002) and the southern end of its distribution in the Central
2015] MARTINEZ-BERDEJA, EZCURRA, AND SANDERS; SEROTINOUS DESERT SPECIES 23
Fig. 1. Ground-level ephemerals (basicarpy); (a) dry dead skeleton and involucre of Chorizanthe rigida, and (b)
whole individual, side and top view of the hygrochastic lignified capsule of Tetrapteron paimeri.
24 MADRONO [Vol. 62'
Desert of Baja California the plant shows a more hygrochastic dehiscence (e.g., Walck and Hi-V
erect habit and can reach 15 cm in height. dayati 2007) that allows seeds to be released*!
Another basicarpic species in this region is preferentially when the capsule is exposed toj|
Tetrapteron palmeri (S. Watson) W. L. Wagner rainwater. Hygrochastic dispersal mechanisms (cid:9632)
& Hoch (Onagraceae), a winter annual that grows allow for seed dispersal through the movement
close to the ground (5-7 mm stalk length) bearing of plant organs or the softening of tissues when !
lignified, rigid capsules with hygrochastic opening wet. These mechanisms rely on the biomechanical
and closing (Fig. lb). Old skeletons, at least one properties of some plant tissues, which may have
year old, have been observed and collected in the compounds that allow them to soften or expand
field. This species is uncommon and grows in as they absorb water, triggering the release of '
open areas, between shrubs, on desert flats in the seeds (van Oudtshoorn and van Rooyen, 1999; i
Great Basin and Mojave Desert where winter Hegazy et al. 2006; Pufal et al. 2010). In the i
rainfall dominates (Baldwin et al. 2002). California deserts, this group is represented by i
Within the basicarpic group, some species two genera, both in the Onagraceae, that tend to |
retain seeds for a shorter-period of time. For inhabit more or less unstable geomorphological :
instance, Chorizanthe spinosa S. Watson (Poly- surfaces such as sand washes and desert dunes, j
gonaceae) is a winter annual that grows spreading Simple wetting experiments we have done, both in
across gravelly surfaces, leaving dense stands of the field and in the lab, show that capsular |
dried skeletons from previous years that retain a opening in these long-term seed retainers is |
few involucres. In the field, most of the involucres triggered by moisture. Eremothera boothii (Dou- j
are released during the following winter season. glas) W.L. Wagner & Hoch (Onagraceae) is a
Its distribution range is restricted to a winter-rain- winter annual that germinates and forms a basal |
only region in the Mojave Desert (Baldwin et al. rosette from which an erect stalk develops (3- \
2002). 35 cm). The stalk bears cylindrical capsules with a i
narrow tip that are persistent and tardily dehis- ^
2. Persistent Plants with Lignified Fruits cent (Fig. 3). This species has two different seed I
morphs coexisting within the same plant: pale
Oxystylis lutea Torr. & Frem. (Capparaceae) is brown seeds, minutely pitted in rows, and coarsely
a summer annual that branches from the base (50- papillate dark brown seeds. There are five |
150 cm) forming a dry spiny structure with two subspecies in the western US that vary in the j
“fairly spheric, smooth, white to deep purple, stiff, degree of woodiness and their distribution area. ^
spine-like nutlets” containing one seed each The three less woody and less serotinous subspe- i
(Fig. 2). The reduction of the silique towards a cies are associated with colder deserts with ;
thick and spinescent style, with a short and stout predictable winter rain: Eremothera boothii subsp. j
pedicel “enclosing a seed, tightly and permanent¬ boothii, E. boothii subsp. alyssoides (Hook. & I
ly, with but a minute pore at their attachment Arn.) W.L. Wagner & Hoch, and E. boothii subsp. !
point” has been considered as an adaptation to intermedia (Munz) W.L. Wagner & Hoch grow on
aridity (litis 1957, p. 83). This species is endemic to sandy slopes or flats in the Great Basin Desert and
Death Valley, forming dry stands in alkaline flats Northwest Arizona. In contrast, the two more
(Baldwin et al. 2002). The seeds are retained for woody and more serotinous species are found in
long periods, but the final release mechanism and the gravelly and sandy soils of desert flats and
the factors that trigger it are unknown. Amaran- washes of the southern, hotter, and climatically more
thus crassipes Schltdl. var. crassipes (Amarantha- unpredictable Mojave and Sonoran deserts: Ere¬
ceae) is a summer-fall annual whose upper fruit mothera boothii subsp. condensata (Munz) W.L.
clusters fall from the plant, while the lower woody Wagner & Hoch and E. boothii subsp. desertorum
clusters from early flowering, located near the (Munz) W.L. Wagner & Hoch (White and
base of the stem, seem to persist on the plant for a Sanders 1997; Felger 2000; Baldwin et al. 2002).
much longer period of time, of unknown dura¬ The genus Oenothera L. includes desert winter¬
tion. This species grows in fine-textured vertisols spring annuals associated to unstabilized sand
of playas and sandy soils adjacent to alluvial dunes or low, sandy mounds more or less
plains and it is distributed in northwestern Sonora stabilized by shrubs in desert regions character¬
and southwestern Arizona (Felger 2000). ized by winter precipitation and dry summers
(Munz 1931; Klein 1970). Oenothera deltoides
3. Gradually Opening Capsules Torr. & Frem. has five subspecies, only one of
which is a strict desert dweller and is strongly
This group includes species that exhibit ligni¬ serotinous suggesting that capsule woodiness is a
fied branches or peduncles holding woody critical factor in its distribution: Oenothera
capsules that open gradually along a year or deltoides subsp. deltoides develops dry, lignified,
even longer. In some species, there is evidence basketlike skeletons that persist for several years :
that the opening of the capsular sutures is bearing lignified capsules that dehisce with
accelerated by moisture, a trait known as moisture (Felger 2000). This spring ephemeral ,
2015] MARTINEZ-BERDEJA, EZCURRA, AND SANDERS: SEROTINOUS DESERT SPECIES 25
Fig. 2. Erect plant with sclerocarpic fruits in Oxystylis iutea.
grows on moving dunes and rolling sand plains in and a cluster of long, slender woody capsules,
the Great Basin, Mojave, and Sonoran deserts that may persist for several years. Ooenothera
(Munz 1931; Klein 1970; Felger 2000; Baldwin primiveris grows on sand flats, playas, and
et al. 2002). Hygrochasy allows this species to gravelly-sandy washes, and is absent from sand
disperse its seeds after rainfall events when it is at dunes, thus this species seems to be adapted to
the upper part of the sand dune, thus allowing less mobile sandy surfaces. It is distributed in the
successful seedling establishment in an unstable Mojave and Sonoran deserts (Felger 2000;
and dynamic landscape. Oenothera primiveris A. Baldwin et al. 2002).
Gray is a winter-spring annual whose dry Semelparous plants in the genus Agave L. form
skeletons consist of part of the taproot and stem, rosettes with tough succulent leaves, and at the
26 MADRONO [Vol. 62j
Fig. 3. Lignified stem and hygrocastic capsules of Eremothera boothii subsp. boothii.
end of their life cycle they produce a large 1982). The dry paniculate scapes of Agave deserti
flowering scape with dry seed-bearing capsules. Engelm. (Agavaceae) persist for two or more
The seeds remain in the capsules on the scape for years after the rosette has died, and its capsules
one or more years as it gradually opens (Gentry gradually open as they weather, releasing seeds
2015] MARTINEZ^BERDEJA, EZCURRA, AND SANDERS; SEROTINOUS DESERT SPECIES 27
into the environment. Agave deserti grows in creosote bush {Larrea tridentata Coville; Zygo-
rocky slopes, and in washes in desert scrub in the phyllaceae). In our fieldwork throughout North
Sonoran Desert, Arizona, and Baja California American deserts, however, we have not observed
(Felger 2000; Baldwin et ah 2002). mericarp retention in creosote bushes lasting for
The annual Datura discolor Bernh. (Solanace- more than a few months.
ae) has spiny, globose capsules that retain seeds The globemallows (Sphaeralcea spp., Malva¬
and gradually turn downwards as the dead plant ceae) fruit is a schizocarp that separates into
skeleton dries. It grows in desert plains, dunes, mericarps, which have an upper smooth dehiscent
and washes in the Sonoran Desert (Felger 2000; part and a lower reticulate indehiscent part, with
Baldwin et al. 2002), and the dry stalks with seed¬ a deep notch between the two sections. Mericarps
bearing capsules often persist for as much as a in desert globemallows contain 1-3 reniform dark
year. brown seeds (Head 1968; Welsh 1980), and the
size of the dehiscent and the indehiscent portion
of the mericarp varies among species (Baldwin
4. Reproductive Dimorphism (amphicarpy)
et al. 2002) (Fig. 4). Six species in the genus
Amphicarpic species display a dimorphic bet¬ Sphaeralcea are found in California deserts
hedging strategy producing two different propa- (Pendery and Rumbaugh 1993; Shriladda et al.
gule morphs that differ in their dispersal and 2012). Four of these species {S. ambigua A. Gray,
survival characteristics: one with higher dispersal S. angustifoHa G. Don, S. emoryi Torr., and S.
and less energy reserves and another with less rusbyi A. Gray) show mericarps with 60-75% of
dispersal ability and higher energy reserves, the carpel open, while the last two {S. orcuttii
representing a high- and low-risk reproductive Rose and S. coulteri A. Gray) show higher seed
strategy (Barker 2005). Enneapogon desvauxii P. retention ability, with only 20-30% of the
Beauv. (Poaceae), a small annual grass, bears mericarp opening. Coincidentally, these last
cleistogamous spikelets in the lower leaf axils two, more serotinous species are strictly endemic
yielding caryopses that eventually germinate in to the Sonoran Desert, while all the others have
situ within their protective sheaths, and chasmo- wider distributions and have been collected
gamous spikelets with smaller unprotected cary¬ largely outside desert environments. Five of these
opses that are immediately dispersed. This species desert globemallows are herbaceous perennials
grows in crevices, rocky habitats, and rocky- with the exception of N. coulteri, which is an
gravelly soils, and is distributed in the Mojave, annual species (Baldwin et al. 2002).
Colorado, and Sonoran deserts (Felger 2000; Similarly, Felger (2000) describes differentially
Baldwin et al. 2002). A similar case of fruit opening mericarps in the desert mallow Horsfor-
dimorphism is also found in Muhlenbergia dia alata (S. Watson) A. Gray (Malvaceae). The
microsperma Trin. (Poaceae), a clumped annual mericarps in this plant have a lower indehiscent
to short-lived perennial grass that grows among chamber that retains seeds until they are dis¬
rocks, along arroyos, and also on sand flats and persed with the entire mericarp, and a dehiscent
playas in the Great Basin, Mojave and Sonoran upper chamber with one or two loose seeds that
deserts, and is also found in coastal sage scrub of disperse when the wings of the dry mericarp split
southern California (Chase 1918; Felger 2000). (Felger 2000). This species is distributed in rocky
Although amphicarpic grasses can be found in slopes, canyons, and arroyos in the Sonoran
the Mojave and Sonoran deserts, reproductive Desert and Baja California.
dimorphism in the Poaceae also occurs frequently
outside arid ecosystems (Campbell et al. 1983).
6. Persistent Fruits
5. Schizocarps with The desert ragweeds {Ambrosia spp., Astera-
Heteromericarps (schizocarpy) ceae) are monoecious plants with commonly two-
flowered pistillate capitula that develop into dry,
Schizocarps are dry fruits developed from spiny, bur-like heads capable of retaining seeds
multiple carpels that, when mature, split up into for some time (Payne 1962). The white bursage
mericarps. In some schizocarpic plants the {A. dumosa [A. Gray] W. W. Payne) forms small
mericarp itself is the dispersal unit, while in hemispherical shrubs with an intricate maze of
others the mericarp forms a small capsule with young stems, many of which die during the dry
two or more seeds, which are shed individually. season retaining the lignified burs within the
Heterogeneity in the shedding ability of the plant’s canopy often for more than one year
mericarps may lead to some seeds being retained (Shreve and Wiggins 1964). This species is
for relatively long periods of time, while others common throughout the driest parts of the
may become readily detached. The ability of Sonoran Desert. The armed ragweed {A. bryantii)
schizocarps to function as seed-retaining struc¬ (Fig. 5) grows in the central Gulf Coast region
tures was recognized by Shreve and Wiggins in Baja California, Mexico, an area of highly
(1964) when describing the dry schizocarps of the unpredictable rainfall patterns. It is a small.
28 MADRONO [Vol. 62
Fig. 4. Schizocarp and mericarp of Sphaeralcea coulteri, showing the reticulate portion holding one
persistent seed.
perennial shrub bearing woody, spiny heads, seeds” (Felger et al. 2001). In the field, capsules
developed from highly transformed capitula that produced in previous years can be easily identi¬
form hard, resistant, flask-shaped involucre cases fied because of their differential weathering. This
bearing 1-2 achenes, with the tips of the species is found in the Sonoran Desert and the
phyllaries forming prominent spines. The spiny eastern Mojave.
heads remain attached to the plant through Other desert plants within the family Solana-
several growing seasons, retaining seeds within ceae develop berries that become dry and
the involucres, which “serve the function of capsule-like, and are able to retain seed for some
armature” (Payne 1962). time. Solarium elaeagnifolium Cav., an introduced
In a remarkable case of evolutionary conver¬ weedy herbaceous perennial that multiplies by
gence, the Sonoran Desert crucifixion thorns, two rhizomes and root fragments, whose berries often
spiny, leafless woody trees with retamoid mor¬ persist as dry fruits (1.0-1.5 cm) that commonly
phology (Shmida 1981), show persistent fruits remain attached to the dead plants. The plants
that dry out while still attached to the plant, and sometimes break off at the base of the stem and
can remain fixed for long periods of time (Felger blow in the wind like tumbleweeds. It is a
et al, 2001). Castela emoryi (A. Gray) Moran & successful dry-land ruderal and distributed from
Felger (Simaroubaceae) is an intricately branch¬ California to South America (Boyd et al. 1984;
ed, leafless shrub with large thorns and very hard Baldwin et al. 2002). A related species, Solarium
and twisted wood. Its fruit is a one-seeded dry hindsianum Benth., is a sparsely branched peren¬
and woody drupe (6 mm) with a flat top and a nial shrub with round dark and light green fruits
rounded base, organized in clusters resembling a (2 cm) that dry out in the plant and persist for an,
seven carpel star-like structure that persists for unknown period. It grows in arroyos and washes
several years in the outer branches (Shreve and in the southern Sonoran Desert (Felger 2000).
Wiggins 1964; Sanders 1998). It is endemic to the Some desert root-parasites have dry capsules
Sonoran Desert where summer rainfall is com¬ that can retain seeds for a season or more. In the
mon or predominant, but extends sparsely into dunes of the Lower Colorado Valley, the desert
the eastern Mojave (Sanders 1998). Similarly, sandfood Pholisma sonorae (A. Gray) Yatsk.
Canotia holacantha Torr. (Celastraceae) has (Boraginaceae) forms stem-pads with many
persistent fruits, fleshy at first “but soon becom¬ circumscissile capsules that dry out gradually
ing woody capsules with five carpels splitting releasing their numerous seeds. Similarly, the
apically into awned valves, each with several inflorescences of the desert broomrape {Oro-
2015] MARTINEZ-BERDEJA, EZCURRA, AND SANDERS: SEROTINOUS DESERT SPECIES 29
Fig. 5. Persistent lignified fruit and seed in Ambrosia bryantii.
banche cooperi [A. Gray] A. Heller; Orobancha- Mejorada 1991; Anderson 2001). These globose
ceae) emerge from the sandy desert plains and cacti often have two modes of seed release: (a)
rapidly dry out, leaving behind a stalk with dry, they can retain fruits for long periods sunken
two-valve capsules that gradually open from the deep within the stem tissue in the axils of the
apex slowly releasing their numerous small tubercles, protected by the spines of the areoles,
seeds. gradually releasing seeds into the environment, or
In the cactus family, seed retention seems to be (b) during rainy years they can extrude some of
a common phenomenon in many desert genera. the fruits, which ripen and turn bright red
Many species of columnar and barrel cacti in offering their seed content to dispersers (Rodri-
different tribes develop spiny-wooly structures guez-Ortega et al. 2006; Peters et al. 2008).
called cephalia where the fruits can be retained Although there are no studies of fruit retention
for a long time, often to be released or exposed to in Californian Mammillaria species, field obser¬
fruit dispersers at the onset of the following rain vations suggest that these two modes of seed
period (Britton and Rose 1923; Bravo-Hollis and dispersal (fruit retention and gradual seed release
Sanchez-Mejorada 1991). In the Californian vs. fruit extrusion and cued release) are common
deserts Echinocactus polycephalus Engelm. & J. in some local species such as M. dioica K.
M. Bigelow (Cactaceae) forms clusters containing Brandegee or M. tetrancistra. Fngelm.
6-50 globose-cylindrical stems (23-30 cm in
diameter each). The tips of the stems harbor
Discussion
densely tomentose fruits that dry after matura¬
tion. As the fruit dries the apical tip opens The adaptive significance of seed retention in
gradually, allowing dispersal of seeds (Chamber- desert plants has been discussed by Fllner and
land 1997; Felger 2000; Baldwin et al. 2002). Shmida (1981) and van Oudtshoorn and van
Ferocactus Britton & Rose species in the Sonoran Rooyen (1999). Other, studies have attributed
Desert often retain fruits. Some chollas, such as different adaptive meaning to serotiny in deserts
Cylindropuntia cholla (F. A. C. Weber) F. M. as allowing to: (a) synchronize seed dispersal to
Knuth distributed in Baja California and Cylin¬ water availability by releasing seeds to rainfall
dropuntia fulgida (Fngelm.) F. M. Knuth form cues (Gutterman and Ginot 1994; Hegazy et al.
chained fruits and the ones from previous years 2006); (b) adaptively regulate the amount of seeds
retain viable seeds. dispersed depending on the within-season
Serotiny is also common in small, tuberculate amount and frequency of rainfall (Friedman et
cacti, mostly in the genus Mammillaria Haw., but al. 1978; Fllner and Shmida 1981; Peters et al.
also in other genera (Bravo-Hollis and Sanchez- 2008); (c) produce an above-ground seedbank
30 MADRONO [Vol. 62
with fractional seed release allowing to spread the them later in synchrony with rainfall pulses, can (cid:9632):
risk of germination over several years (Ellner and be highly advantageous for plants depending on \
Shmida 1981; Giinster 1994; Gutterman and rare and erratic pulses of water for their survival.
Ginot 1994; Narita 1998; Rodriguez-Ortega
2006; Peters et al. 2008); (d) keep seeds enclosed Acknowledgments :
in dispersal-restricting seed containers protecting We thank Mitch Province for the illustrations for this si
them from predation (Ellner and Shmida 1981; publication. Sula Vanderplank, Benjamin Wilder, and '
Narita and Wada 1998); and (e) retain the Richard Felger helped us revise the list of serotinous i
parental site, a proven microhabitat for successful species. This article is based on the first chapter of the
establishment (Friedman and Stein 1980; Ellner first author’s dissertation. f
and Shmida 1981; Giinster 1992, 1993; Hegazy
Literature Cited
and Kabiel 2007).
Serotinous species occur in different deserts of Anderson, E. F. 2001. The cactus family. Timber !
the world (e.g., Giinster 1992 for the Namib and Press, Portland, OR.
Gutterman and Ginot 1994 for Israel) where Baldwin, B. G., S. Boyd, B. J. Ertter, R. W. i,
Patterson, T. J. Rosatti, and D. H. Wilken i
common seed retention syndromes observed in
(eds.). 2002. The Jepson Desert Manual: vascular
serotinous species of the Sonoran and Mojave
plants of southeastern California. University of '
deserts, such as basicarpy, amphicarpy, and
California Press, Berkeley, CA. !
hygrochastic capsules, have also evolved. These Barker, N. P. 2005. A review and survey of ?
different dispersal syndromes seem to be related amphicarpy, basicarpy and geocarpy in the African :
to particular geomorphological desert features. and Madagascan flora. Annals of the Missouri
For instance, Chorizanthe rigida, the most Botanic Garden 92:445M62. !
common basicarpic winter annual in the Mojave Boyd, J. W., D. S. Murray, and R. J. Tyrl. 1984. (cid:9632)
Silverleaf nightshade. Solarium elaeagnifoUum, ori- ;
and northern Sonoran deserts, grows mainly in
gin, distribution and relation to man. Economic (cid:9632)
desert pavements. Coincidentally, other basicar¬
Botany 38:210-217. i
pic plants in different world deserts and in
Bravo-Hollis, H. and H. SAnchez-Mejorada.
different families such as Acanthaceae, Astera- 1991. Las cactaceas de Mexico. Vol. III. Universi-
ceae, and Brassicaceae also seem to establish dad Nacional Autonoma de Mexico, Mexico City. ;
preferentially in pavements (Friedman et al. 1978; Britton, N. L. and J. N. Rose. 1923. The Cactaceae. i
Ellner and Shmida 1981; Gutterman and Ginot Dover Publications. Inc., New York, NY.
1994; Narita and Wada 1998; van Oudtshoorn Chamberland, M. 1997. Systematics of the Echino- |
cactus polycephalus complex (Cactaceae). System- •
and van Rooyen 1999). Similarly, the lignified
atic Botany 22:303-313. j
basket-like structures or “bird-cages” of the
Chase, A. 1918. Axillary cleistogenes in some Amer¬
Onagraceae in mobile sand dunes of the Mojave
ican grasses. American Journal of Botany
and Sonoran deserts is remarkably convergent 5:254-258. i
with the growth morphology of Artemisia L. Ellner, S. and A. Shmida. 1981. Why are adapta¬
species (Asteraceae) in desert dunes in China (Ma tions for long-range seed dispersal rare in desert ;
et al. 2010). plants? Oecologia 51:133-144. |
Moreover, there seems to be an association Enright, N. J. 1998b. The ecological significance of |
canopy seed storage in fire-prone environments: a j
between the low-lying basicarp plants and winter
model for re-sprouting shrubs. Journal of Ecology ;
rains, and between taller and erect plants with
86:960-973.
lignified fruits and summer rains. All of the
-, R. Marsula, B. B. Lamont, and C. Wissel. |
basicarpic plants in the floras we reviewed are 1998a. The ecological significance of canopy seed
distributed mostly in the Mojave and northern storage in fire-prone environments: a model for
Sonoran deserts, where rain falls predominantly non-sprouting shrubs. Journal of Ecology
during winter, while the taller seed retaining 86:946-959.
annuals occur largely in the eastern and southern Felger, R. S. 2000. Flora of the Gran Desierto and
Rio Colorado of Northwestern Mexico. The :
Sonoran Desert outside California, where sum¬
University of Arizona Press, Tucson, AZ.
mer monsoon rains are important.
-, M. B. Johnson, and M. F. Wilson. 2001. The
In conclusion, there is a striking convergence
trees of Sonora, Mexico. Oxford University Press,
of dispersal syndromes in distant deserts that are, New York, NY.
to a large extent, taxonomically unrelated (e.g., Friedman, J. and Z. Stein. 1980. The influence of ;
Ellner and Shmida 1981 and van Oudtshoorn and seed-dispersal mechanisms on the dispersion of
van Rooyen 1999). In the same way as the pulses Anastatica hierochuntica (Cruciferae) in the Negev
of wildfires have selected seed-retaining plants in Desert, Israel. Journal of Ecology 68:43-50.
-, N. Gundermann, and N. Ellis. 1978. Water
fire-driven ecosystems, the unpredictable pulses
response of the hygrochastic skeletons of the true
of water abundance against a background of
Rose of Jericho {Anastatica hierochuntica L.).
extreme water scarcity seem to have played an
Oecologia 32:289-301.
important role in the evolution of serotinous Gentry, H. S. 1982. Agaves of continental North
desert plants. Retaining seeds well protected America. The University of Arizona Press, Tucson, ,
within the lignified maternal tissues, to release AZ. i
