Turgrass Report

8/13/2019 Turgrass Report

1/26

Origin, Biogeographical Migrations and Diversifications of Turfgrasses 1

ORIGIN, BIOGEOGRAPHICAL

MIGRATIONS AND DIVERSIFICATIONSOF TURFGRASSESJames B Beard1

Executive Summary

Whether a turfgrass species is characterized asnative or naturalized to North America has beenbased on world-wide simplistic observationsfocused on where the greatest genetic diversityoccurred, termed center-of-origin. Research infor-mation as to dating and locations of subsequentmigration and diversification has been minimaldue to a lack of needed research technologies.Intercontinental migration of grasses has beenassumed to have been unlikely due to oceanicseparation. Recent development of paleobotanicalstudies using ultrastructural electron microscopictechniques and stable carbon isotope datinginstrumentation and research procedures, plus

molecular phylogenetic research and cladisticbiogeographic analysis of large data sets areclarifying our understanding of migration patternsand dating of multiple secondary centers-of-originfor grasses.

Pre-anthropological intercontinental migration ofgrasses is now being documented as more sig-nificant than previously assumed. Global heating/cooling phases and shifts in sea level appear tohave facilitated oceanic island hopping. At varyingtimes, these bridge migrations may have involved

the northern Europe to North America routevia Greenland, Bering Bridge between Asia andNorth America, southeast Asia to Australia viaNew Guinea, South America to North America viaCaribbean and later via Panama Bridge, and Africa-Europe via the Gibraltar Straits. Also, the potentialfor transoceanic migrations is being reconsidered.

Primitive ancestral grasses are now proposedto have appeared during the Late Cretaceousbetween 65 and 96 mya (million years ago) inGondwanan Africa. The ancestral Pooideae areestimated to have migrated to the steppes ofLaurasian Eurasia during the Eocene ~38 to47 mya. Taxonomic divergence of the base C

3

Pooideae group appears to have been initiated inEurope ~26 to 33.5 mya. The base C

4Pooideae

apparently arose in Africa ~30 to 33 mya, followedby migration to West Gondwana South Americaand to East Gondwana India and Australia.

Diversification led to the emergence of an ancientPoeae group known as the fine-leaf fescues(Festuca) in central-Europe during the mid-Miocene ~13 mya. Subsequent migration occurred

via the mountains of central and eastern Asia,across the Bering Land Bridge into North America,southward via the western mountains, over thePanamanian Land Bridge, and across the Andesto Patagonia. This occurred between ~3.8 and 10mya, which is before the anthropological effectsof humans. Clearly, the fine-leaf fescues are nativeto North America, migrating eastward after theice age glacial melt ~1 mya. Similar investigations

with other turfgrasses may clarify the migrationrouting and diversification dating of other turf-grass species. Thus, the current status of turfgrassspecies in terms of native or anthropologicalnaturalization is presented in this paper and sum-marized in the following table.

1 Professor Emeritus, Texas A&M University and International Sports Turf Institute, College Station, Texas, 77840; e-mail [email protected]. This electronic version is being published by the Michigan State University Press in a book titled Turfgrass His-tory and Literature. Copyright 2012, James B Beard.

Research Report | SR132


2/26

2 Origin, Biogeographical Migrations and Diversifications of Turfgrasses

Summary of native and naturalized categories of 24 turfgrasses found in North America, based on

current knowledge.

*Needs further biogeographical and phylogenetic research to confirm.

Native/Naturalized Categories Grass Genus and Species Turfgrasses Common Name

Native, based on biogeo-

graphical, phenotypic, andphylogenetic studies.

Festuca rubra

Festuca trachyphylla

Festuca ovina

red fescues

hard fescue

sheep fescue

Native, based on phenotypicand genetic assessments.*

Axonopus compressus

Axonopus fissifolius

Bouteloua curtipendula

Bouteloua gracilis

Buchloe dactyloidesStenotaphrum secundatum

broadleaf carpetgrass

common carepetgrass

side-oats gramagrass

blue gramagrass

American buffalograssSt. Augustinegrass

Possible native, based onphenotypic assessments andallied species biogeographical,phylogenetic studies.*

Agrostis capillaris

Agrostis stolonifera

Agrostis canina

Poa pratensis

colonial bentgrass

creeping bentgrass

velvet bentgrass

Kentucky bluegrass

Possible naturalized, following

anthropological introduction.*

Eremochloa ophiuroides

Lolium multiflorum

Lolium perenne

Paspalum vaginatum

Poa trivialis

Schedonorus arundinaceus

Zoysia japonica

Zoysia matrella ssp. matrella

Zoysia pacifica

centipedegrass

annual ryegrass

perennial ryegrass

seashore paspalum

rough bluegrass

tall fescue

Japanese zoysiagrass

manila zoysiagrass

mascarene zoysiagrass

Undocumented, needsresearch

Cynodon dactylon ssp. dactylon

Poa annua

dactylon bermudagrass

annual bluegrass


3/26


Introduction

Understanding the relatively recent research ingrass species evolution and development hasdictated revision of how native and naturalizedturfgrass species are viewed, especially in North

America. The supporting research for this updat-ing is reviewed herein.2

Native Turfgrass Species.Websters ThirdNew International Dictionary defines native assomething indigenous to a particular locality.Indigenous is defined as native and as originatingor developing or produced naturally in a particularland or region or environment. The emotive as-sociated terminologies relative to native that havebeen used include naturalized, alien, exotic andnon-native. Criteria for classifying native spe-

cies that have been utilized or proposed includehistorical, geographical, economical, behavioral,sociological and/or political considerations. Thelatter four involve value judgments based on anarbitrary frame time that results in controversydue to the diversity of human preferences andneeds (53). Thus, the native aspects of turfgrassesaddressed herein will rely on time and geographicdimensions documented by sound, hard science.

There are proponents who consider the plant spe-cies present in America when Europeans arrived as

the natives that have persisted from time imme-morial free from human disturbances. However,recent research indicates there are woodland areasthat have developed subsequent to anthropologi-cal disturbance during the late-Holocene at least4,000 years ago (80). These mound-building, early-American populations were active in domesticatedcrop propagation involving intensive land use byfire to remove forested areas. Such anthropologicalimpacts on plant species disturbance and reinva-sion by intermediate succession species have beenrecently documented for regions in southeastern

and in north east central North America (33, 80),and others probably will be found.

One can only speculate as to the grass speciesthat would have been naturally introduced and

persisted in recent times if human disturbance hadnot occurred. Disturbed environments can havelong-term or short-term effects on plant com-munity composition depending on the degree and

duration of the disturbance event. Disturbance canbe a natural aspect of plant ecosystems as causedby drought, fire, disease, insect, glaciation, heatstress, freeze stress, volcanic smoke, soil deposi-tion, soil salt level, animal pressures, etc. Defininga native plant based on a fixed point in time, suchas pre-Holocene, pre-Neolithic, or pre-Europeancolonial, is unrealistic as it assumes no non-humandisturbances would have occurred subsequently.It also fails to acknowledge humans as a compo-nent of the ecosystem. Historically, the speciescomposition of most plant communities has been

a continuous, dynamic process of transitionaldiversification and recovery. It is likely the naturaldistribution of plant communities still wouldbe different even if human intervention had notoccurred. Similarly, species move geographicallyin response to environmental changes caused bothnaturally and by human disturbances. Thus nativesites should not be viewed as fixed geographicalareas that existed prior to human activity. Also,the premise stated by some individuals that nativeturfgrasses inherently possess lower culturalrequirements, resource inputs, and/or water userates, plus better human benefits than non-nativespecies is not valid (53).

Application of the native terminology for grasseshas varied over the past century, and previouslyemphasized the effects of tectonic processesthat resulted in assumed geographic barrierssuch as oceanic separation of continents. Somegrass taxonomy and flora books include a geo-graphic description that proposes a continent(s)or region(s) where each species is native. In theearly 1900s there were North American texts ongrass taxonomy that referred to grass species, suchas the Agrostis, Festucaand Poa, as natives. Then bythe mid-1900s most grass taxonomic, flora andother texts listed such species as native to Eurasia.

2Assistance of Michigan State University Library personnel in the Turfgrass Information Center is acknowledged, includingliterature acquisition by Peter Cookingham and Michael Schury, and artwork by Aaron Tomak. Also, critical reviews of thesection by Jeff V. Krans, Emeritus, Mississippi State University, William A. Meyer, Rutgers University, Robert B. Shaw, TexasA&M University, and Robert C. Shearman, Emeritus, University of Nebraska, are appreciated.


4/26


This change in the center-of-origin concept wasbased on plant exploration that indicated thegeographic region thought to possess the greatestmorphological diversity. Unfortunately, the truecenter-of-origination for a species may no longerexist botanically due to severe, extended droughtas occurred in Africa or due to ice age glacial

presence as in the Northern Hemisphere. Also, theoceanic separation of continents is not proving tobe the migration barrier once assumed (48, 85).

The development of molecular phylogenetictechniques during the past two decades, involvingDNA sequencing instrumentation and unique phe-netic and cladistic analyses via computer programsfor large data sets, have drastically changed ourunderstanding of when and where diversificationsof grass genera, subgenera, species and subspe-cies occurred. Thus, an update of the native or

naturalized status of the major turfgrass species isaddressed herein.

Naturalized Turfgrass Species.The termnaturalized turfgrass species is defined herein asa plant that is introduced, becomes establishedand persists without direct human inputs. Theintroduction may be unintended or intended. Anintroduced, heterozygous species may diversifyand naturalize as a local ecotype that is welladapted, functionally valuable, and non-invasive.Also, multiple independent origins of similar

genotypes have occurred in widely separated butsimilar environments, as has been documentedfor Agrostis capillaris,Agrostis stolonifera, and Poa annua(57). The plant community composition is inher-ently dynamic, with preservation of the status quoon a long-term basis unlikely. It is natural to haveboth migration/introduction and naturalizationof species. Anthropological related naturaliza-tion contributes to species diversity of plantcommunities.

Taxonomy.The grass taxonomy employed herein

is that of Barkworth et al. (6, 96, 97). The clas-sification system for grasses is Kingdom - Plantae,Phylum - Magnoliophyta (syn. Division), Class-Liliopsida (syn. Monocotyledonae), Subclass -Commelinidae, Superorder-Poanae, Order - Poales,and Family-Poaceae (syn. Gramineae). Subfamilynames end in -oidea, tribes in -eae, and subtribesin -inae.

The traditional grass taxonomic system is basedon morphological similarities, especially theinflorescence. A more recent classification systemis cladistics, or phylogenetics systematics in

which groups or clades are organized based onrelative dating of common ancestors with shareddiversity of anatomical, physiological, biochemical

and morphological features. Basically a clade mayencompass all descendant species of an ancestor.Two major grass clades are BEP encompassingthe Bambusoideae, Ehrhartoideae, and Pooideaesubfamilies and PACCMAD encompassing thePanicoideae, Arundinoideae, Chloridoideae,Centothecoideae, Micrairoideae, Aristidoideae,and Danthonioideae subfamilies (15, 32, 42, 43, 77).

The BEP clade contains exclusively C3grass

species, while the PACCMAD clade includes C4

species, as well as all known C grasses. The latter

are mainly distributed within the Chloridoideae,Aristidoidae, and Panicoideae subfamilies. Thecrown node for the BEP clade is estimated to be ~10 million years older than that of the PACCMADclade (17). Numerous subclades become evidentfrom the cladistic applications (2, 15, 25, 26, 39,48, 51, 58, 62, 67, 85, 86), resulting in taxonomicclassifications that more nearly depict evolutionof the grass family. Cladistic classification of themonocotyledons indicates the Joinvilleaceae area sister group to the Poaceae within the SubclassCommelinidae (35, 51, 86, 89).

Plant Evolution Phases.The geophysicalaspects of grass species evolution involve a (a)primitive ancestral center-of-origination, (b) earlydiversification, (c) migration or dispersal, and (d)species secondary centers-of-origin or diversifica-tion in order to adapt and survive changes. Thesechanges include environmental (temperature,

water, irradiation, and carbon dioxide), edaphic(soil texture, pH, nutrients, and salts), and biotic(animal grazing, human activities, and pests).There also are continuing intraspecies diversifica-tion regions in response to current natural andhuman environmental disruptions. Accordingly,micro centers-of-diversification occur involvingsmall areas where mutations and hybridization aresignificant as represented by the presence diploid,triploid, tetraploid, hexaploid, and even octoploidplant species (101).


5/26


Previously a sometimes ill-defined center-of-origination had been considered phenotypically tobe a region where the greatest diversity of a grassspecies occurs. More recently, either confirma-tion or major adjustments in dating and locationhave been made possible by more sophisticatedpaleobotany using ultrastructural electron mi-

croscopic techniques plus stable carbon isotopedating instrumentation and research procedures.Actually, the secondary species centers-of-originand/or diversification may be more important thanthe center-of-origination (48), especially if thoseancestors in the center-of-origination becameextinct as a result of adverse climatic changes,such as the severe drought that occurred in Africa.Also, key secondary centers-of-diversification fortemperate C

3grasses were formed after subsidence

of the last glacial age.

Current data indicate certain morphologicaldiversifications of grasses have occurred at least23 mya (million years ago) after the origin ofa particular character (51). Diversification is adynamic ongoing process with multiple secondarymicro-centers-of-origin. A grass population has thepotential for further differentiation that leads tobetter genetic adaptation to a specific environmentby natural selection.

Early Plate Tectonics. Grass-dominated ecosys-tems now cover more than one-third of the earths

land surface area. This was not always the case.Early evolutionary history of primitive ancestralgrasses and their broad migration patterns arethought to have been influenced by shifting posi-tions of land masses (27) and seas that created andeven destroyed environments where the ancestralgrasses originated or migrated. Plate tectonic theo-

ry has been advanced by new geological evidenceand contributes to concepts of angiosperm-Poaceae distributions. The supercontinent Pangeaformed ~500 mya. Its configuration as it existedin the medial Cretaceous prior to continentalbreakup is shown in Figure 1. Pre-continentalseparation of Pangaea with possible ancestral grassmigrations also are shown.

Pangaea split into Laurasia, now North Americaand Eurasia, and into Gondwana, now SouthAmerica, Africa, Antarctica and Australia, dur-

ing the late-Mesozoic era ~160 mya. A landconnection between Gondwanan-Africa andLaurasian-Europe was present in the westernMediterranean region. The early Laurasian landconnection between Europe and North America istermed the North Atlantic Land Bridge. Gondwana

was characterized by mild temperatures and ahuge range of flora and fauna for millions of years.The early West Gondwana formation may haveallowed South America to be more directly landaccessible to primitive ancestral plant migrationfrom Africa than from Laurasian North America.


6/26


Figure 1.Depiction of the probable relative positions of the Laurasian and Gondwanan landmasses in the medial Cretaceous ~100 mya (adapted from Smith, Briden and Drewry, 1973), and

possible broad migration patterns of primitive ancestral grasses (PA), plus later migration of

cool-season ancestral grasses (CA) and warm-season ancestral grasses (WA).

CA

PA

WA


7/26


Intercontinental Plant Migration. The move-ment of plant species between continents anddirectionally across large continental areas isreferred to as migration. Transcontinental disper-sals have been found to occur earlier and morefrequently than was once assumed (48, 85). Wind,birds, animals and/or floating debris may have

contributed to such dispersals. Species distribu-tions and multiple centers-of-diversification tendto be influenced by conditions existing since thePleistocene. Direct intercontinental plant migra-tion of primitive ancestral grasses was possibleup to or following specified dating as extensivelyreviewed by Raven and Axelrod (72) (Table 1).Patterns of potential intermittent ancestral plantmigration to North America (72) may have in-

volved a Laurasian direct land route from Europe,

an indirect land route from Asia via the BeringLand Bridge, and a more recently formed landroute from South America via the PanamanianLand Bridge (Table 1).

Note that moderate biogeographic plant migrationby oceanic island-hopping probably occurred via

birds, wind and/or flotation for a significant timefollowing geologic dated continent separation.A narrow gap interspersed with volcanic islandsbetween Africa and South America presumablycould have allowed primitive flora migrations upinto the Paleocene (58, 72). It has been proposedthat tropical grass subfamilies may have continuedto migrate until continental separation reached a

water gap of 745 miles (1,200 km) during the firsthalf of the Tertiary ~50 mya (28, 72).

Table 1. Summary of when possible early intercontinental plant migration patterns for primitive an-cestral grasses could have occurred (72).

EventOccurrence

Specific ContinentalContact Event

Event Dating(millions of years ago)

Last

Last

Last

Last

Last

Africa and India

Africa and South America

Africa and Eurasia, prior to Miocene event

Europe and North America

South America to Australia via Antarctica

~100 mya - late-Lower Cretaceous

~90 mya - early-Upper Cretaceous

~63 mya - early-Paleocene

~

49 mya - mid-Eocene

~38 mya - mid-Eocene

First

First

First

India contacts Asia

reestablished between Africa and Eurasia

South America and North America

~45 mya - early-Eocene

~17 mya - mid-Miocene

~5.7 mya - late-Miocene


8/26


Major island-hopping of animals and grasses isprobably represented by southeast Asia - Australia

via New Guinea ~15 mya, and by South America -North America via an intermittent land connection~10 to 12 mya (72). Migration from Asia-Europe toNorth America via the Bering Land Bridge has oc-curred since ~55 mya (72). The ancestral Bovidae

migrated to North America from Europe-Asia viathe Bering Land Bridge (73). There also was aland uprising to form the Gibraltar Strait Bridgebetween Europe and Africa ~5 mya by whichBovidae migrated to Africa. Oceanic island-hop-ping between South America and North Americamay have occurred from ~45 mya. Mountainhop-ping from Europe to Asia to North America toSouth America may have occurred starting at least10 mya for Agrostis,Festuca, and Poa(39, 48, 72).

Primitive Ancestral Grasses. Definitive

evidence is limited concerning the continentalcenter-of-origination for primitive ancestralgrasses. Fossil records for the grass family Poaceae

within the angiosperms and their ancestors arevery incomplete. Based on paleobotanical evi-dence, including silicified plant tissues termedphytoliths and stable carbon isotope studies,primitive ancestral grasses appeared rather latein the earths history at somewhere between 55and 70 mya (43, 48, 51). It has been proposedand supported by phylogenetic analyses that theArundinoideae was the ancestor from which thecool-season monophyletic Pooideae arose (28, 52).

Available evidence suggests the primitive ances-tors of Poaceae occurred in the tropical forestsand fringes of Gondwanan-Africa (17, 28, 58, 86).An extensive review of pollen fossil records byMuller (64) indicates basal Poaceae were presentin the Paleocene epoch ~55 to 60 mya in centralto eastern Africa and east-central South America.Macro-fossil plant remains from a formationin western Tennessee suggest the presence of acommon ancestor for the Poaceae under tropical,seasonally dry conditions ~ 55mya (30).

This is a significant finding, relative to nativegrass species evolution in North America. Thecrown node of the BEP & PACCMAD clades hasbeen estimated phylogenetically at ~57 mya (17).Phytoliths preserved in coprolites from centralIndia revealed five extant Poaceae subcladespresent during the Upper Cretaceous ~65 to 70mya (70). Molecular phylogenetic and cladistic

biogeographic analyses propose a dating range ofPoaceae at Late Cretaceous ~65 to 96 mya (16, 17,26, 35, 58).

Both diversifications and migrations of grasseshave been influenced by changing regional envi-ronmental, edaphic and biotic influences. Included

were changes in tectonic plate processes, iceage glaciation, volcanic activity, tropical domi-nance, sea level, fire, water availability, favorabletemperatures, seasonality, competitive flora andfauna. Note that ice age climatic change during thePleistocene was particularly disruptive in terms ofgrass species diversification and migration in theNorthern Hemisphere.

Diversification.Phytogeographical analyses sug-gest early differentiation of the lineages for tribesof the Poaceae may have started by the end of the

Upper Cretaceous (26, 58). The Pooideae probablydiversified initially in temperate environments athigh latitudes and high altitudes in the tropics(58). From ancestral origination in fringe-forestedregions, there appears to have been further evolu-tion to savannas, and then to temperate steppesin the case of the Pooideae. The C

3cool-season an-

cestral grasses are estimated to have arisen duringthe Eocene ~44 to 55 mya (30, 95). The Pooideaeare estimated to have migrated to the steppes ofEurasia ~38 to 47 mya (17). Grass pollen fossils aremore abundant during this epoch (64).

The C4physiological characteristics of warm-

season ancestral grasses evidently appeared as atleast 12 distinct events and locations starting inthe Oligocene ~30 mya and subsequently thru 15mya (16, 17, 43, 51, 54, 86). The C

4warm-season

ancestral grasses of the Panicoideae and theChloridoideae are estimated to have originated~26 mya and ~29 mya, respectively (17). Theemergence of C

4grasses was associated with a

drop in atmospheric carbon dioxide (CO2) levels

(16, 37) and/or seasonally drier climates (28, 56).

Macrofossils of Chloridoideae grass leaves fromKansas indicate C

4Kranz leaf anatomy existed

in the Miocene ~5 to 7 mya (97). Also, evidenceindicates that C

4grasses expanded in the Americas

during the late-Miocene (56).

Early grasses eventually became significant compo-nents of plant communities in the dryer savannas,steppes, and prairies. The increasing dominanceof grasses was probably aided by periodic


9/26


lightning-induced fires that destroyed mosttree and shrub competitions, while the grassessurvived via basal tillering. Actually the dry grassbiomass provided fuel for the fires.

It is postulated that since Gondwana phytogeo-graphically separated into the present major

continents, numerous distinct grass diversifica-tions have occurred on four separate continents.The original ancestral grasses have now evolvedinto a large family of angiosperms with ~40 tribes,~800 genera, and ~11,000 species (26).

Migration.Grasses had eventually dispersed toall continents ~60 million years after their ances-tral Gondwanan-Africa origin (17). Phylogeneticstudies suggest the first migration within thePooideae from Eurasia to North America oc-curred ~38 mya via the North Atlantic Land

Bridge when there was a global warming trend(17). Subsequently there is evidenced that otherBEP taxa migrated from Europe via Asia to NorthAmerica by the Bering Land Bridge (48).

Modes of seed dispersal away from the parentplant can occur by animals, gravity, wind and

water. Certain grass species possess characteris-tics that allow either internal or external transportby animals. Internal mechanisms can occur via thedigestive tract, primarily of large grazing animals(66, 71). The ingestion and internal passage of

viable seeds through the digestive systems of ani-mals has been documented for C3grasses Agrostis

stolonifera, Festuca rubra, Festuca elatior, Poa annua, Poacompressa, and Poa pratensis(34) and for C

4grasses

Axonopus fissifolius(19, 65), Buchloe dactyloides, Cynodondactylon, and Paspalum notatum(19).

Certain chaff-like grass seeds facilitate externaltransport on the fur coats and hairy hides of mobileanimals. Seeds with distinct awns, hairy lemmas,and/or sharp-pointed florets allow penetration inanimal hair and resist easy withdrawal (24).

Many grasses adapted for turfgrass purposes havevery small, light-weight seeds that can migrate viawind. For example, the approximate number ofseeds per pound (0.45 kg) for Agrostis capillaris> 5million, Cynodon dactylon> 1.5 million, Poa pratensis>1 million, and fine-leaf Festuca> 400,000 (10). Largedust storms from Africa to the Americas may havefurthered intercontinental dispersal of certaingrass seeds.

The same chaff-like, light-weight seed character-istics also aid migration in flowing water downstreams and rivers, especially in association witheroded soil. Stenotaphrum secundatumseed has aninflorescence structure that enhances flotation onocean currents between islands and along coastalshorelines (79).

The presence of a chemical germination inhibitorin the seed is another mechanism by which somespecies of grass seeds extend the duration forpotential migration. Poa pratensisis an example

with modern cultivars having seed germinationdelays of 3 to 4 months (10) following maturation.Certain earlier ancestral grasses probably hadlonger germination inhibition periods due to ahigher inhibitor content and/or greater resistanceto inhibitor degradation.

Some grass species have what is termed hard seed,in which the seed coat is impermeable to waterneeded to initiate germination. Typical turfgrassspecies with hard seeds include Cynodon dactylon,Eremochloa ophiuroides, and Zoysia japonica(10).Germination can be improved by mechanical oracid scarification to open the seed coat barrier.Either the presence of a hard coat or an inhibitorin seed could facilitate distance dispersal of suchgrass species in the digestive systems of birdsand animals, especially herbaceous-grass feedinganimals (24).

Grazing Mammals and Turfgrasses.The an-cestral species for some turfgrass species evolvedin association with herbivorous grazing mammals.Early, now extinct browsing ungulates known asCondylarths evolved while feeding on ancestralC

3grass terrestrial ecosystems during the early

Paleocene ~65 mya (8, 42). Subsequently, duringthe early-Eocene ~55 mya, early herbivorous ru-minant Artiodactyls arose. The Bovid subfamiliesexhibited a rapid diversification ~23 mya (63). TheBovidae family, with a distinct tooth structure,

arose in the late- Miocene ~5 to 9 mya. Evolvingin Eurasia were cattle, antelope and bison of thesubfamily Bovinae, plus goats, sheep, water buffaloand musk-ox of the subfamily Caprinae (63, 95).

Early grasses persisted as a minor componentof a forested plant community for a long time.Eventually, ancient grass-dominated ecosystemsdeveloped in certain open regions ~5 to 6 mya as aresult of significant changes to a drier environment


10/26


that caused a decline in tree populations (91).During this time, certain herbivorous mammalsalso were evolving with mouth parts adapted tograzing more closely, and also with high-crownedteeth and/or constantly-growing teeth needed forgrazing on grasses with high phytoliths or silici-fied fibers (61). Consequently, there was selection

toward grass species in certain regions that werestructurally adapted to survive severe defoliation(88).

While open-habitat grasses exhibited taxonomicdiversification in North America at least 34 mya,phylogenetic studies suggest they did not becomeecologically important until formation of thesavanna-like Great Plains 23 to 27 mya (90). Amajor expansion of C

4grasses occurred during the

late Miocene ~6 to 8 mya during a major climatechange to a dryer environment and lower atmo-

spheric CO2levels (23, 37, 56). Intercontinentaldistribution of both C

3and C

4grasses stabilized

during the late Miocene ~6 mya (61).

Carbon dating of herbivorous mammalianskeletons and attached grass remnants by paleo-botanical studies and DNA sequencing confirma co-migration and even co-evolution among anumber of grazing mammals and certain peren-nial grasses (16, 24). The interrelationship oflow-growing grasses and herbivorous mammalscontinued over an estimated period of ~10 to 20

million years (8). The result was a number of grassspecies having (a) leaves with basal meristems,(b) shoots with short basal internodes, and (c)prostrate, creeping growth habits via lateralstems termed stolons and rhizomes. Evolution ofthese morphological adaptations in some grassesallowed subsequent use for turfgrass purposesinvolving frequent, low mowing.

Some centers-of-diversification for temperategrasses are of more recent post-Pleistocene de-

velopment ~2 to 1 mya due to glacial effects from

the last ice age. Examples are the North Americannortheast and midwest regions and the higheraltitude meadowlands of Central Europe.

Human Dispersal. Intercontinental human grassdispersals may have occurred even earlier thanNew World colonial times. Over 600 years ago

world voyagers and global explorers may havedumped from their ships at various world-widelocations sweepings containing straw and hay

bedding composed primarily of grasses. Latercolonists traveling via boat to the New World,primarily from Europe, brought grasses for agrar-ian forage and pasture purposes. These introducedgrasses had been selected for more than 400 yearsbased on a higher yield or biomass productionneeded for feeding herbivorous domesticated

animals (81). These early colonists preferred thetaller-growing, high-yielding, introduced grassesfor agrarian purposes. The European forage andpasture grasses were less desirable as turfgrasses,especially in early times of laborious manual mow-ing. Many European-introduced grass genotypesnaturalized in North America through intraspe-cies diversification and natural selection over aperiod of 300 to 400 years. These grasses becameinterspersed with pre-colonial native grass com-munities, especially in eastern North America. Forexample, a good germplasm source for turfgrass

selection is in old cemeteries that have beenmowed regularly, but typically not irrigated orfertilized. Clarification as to the specific geneticsources from which many contemporary turfgrasscultivars were derived will require molecularphylogenetic research.

Modern Diversification.Globally, there are ~40 grass species utilized as turfgrasses to varyingdegrees. Most are heterozygous with inflorescencefertilization by wind-aided cross-pollinated. Theresult is a wide range in diversity with many grassecotypes that have specific adaptation potentials tothe numerous global variations in the environmen-tal, edaphic and biotic components contributingto the broad array of ecosystems. Furthermore thediversification process for individual grass speciesis ongoing with new genotypes emerging and somegenotypes possibly becoming extinct if poorlyadapted to the specific environment in certainecosystems (81).

To the untrained observer a turfgrass community,such as a lawn, may appear to lack diversity. Thisis because the basic leaf characteristics are moresimilar in shape, orientation and color comparedto the broad-leaf dicotyledonous species such astrees, shrubs, and flowers. Actually the geneticdiversity is substantial in most mature turfgrasslawn communities. It is a key to the capability ofgrasses to recover and survive as perennials under

wide seasonal variations in temperature, water,shade, traffic, and pest stresses.


11/26


12/26


COOL-SEASON TURFGRASSES

The primitive ancestral center-of-origination forcool-season grasses (Pooideae) is thought to havebeen from the tropical forest margins of Africaat higher altitudes (28). The unique evolutionaryfeature possessed by Pooideae was adaptationto cold climates that allowed migration to thetemperate steppes of Eurasia (28). Subsequentlythe Pooideae may have emerged under a tree-shrub dominant, temperate ecosystem withsufficient precipitation for sustained growth andpossibly survival during occasional short periodsof droughty conditions. Taxonomic divergenceof the base Pooideae group appears to have beeninitiated after a global super-cooling period ~26to 33.5 mya (78). Diversification also was probablycharacterized by a cool temperate climate, plus

reasonably good precipitation and soil fertility.Cool-season grass diversification in Eurasia mayhave been greater in the mountainous areas whereshade from trees was reduced. Plant explorers3report greater diversity within the Festuca, PoaandAgrostisspecies in Europe-Asia at altitudes above3,000 feet (915 m).

The cool-season turfgrasses discussed herein aretaxonomically classified in the Pooideae, with C

3

physiology (96). Within the Pooideae there aretwo supertribes, including Poodae, and seven

tribes, including Poeae. The Pooideae includes ~3,300 species. The Poeae encompass ~115 generaand ~2,500 species (6), and occur with a high spe-cies frequency percentage in the higher latitudesand higher altitudes where summer and wintertemperatures are colder (92). The cool-seasonturfgrasses occur in the temperate climates ofboth the northern and southern hemisphere andin mountains of the tropics, with an optimumtemperature range of 60 to 75F (16 to 24C) (10,11). Migration bridges of certain C

3cool-season

perennial grasses evidently occurred by mountain-hopping. The likely migration route for the freezetolerantAgrostis, Festucaand Poaspecies intothe South American Andes was via the NorthAmerican, Asian and European mountains (18,48). In North America these three genera typicallyhave their largest range of species diversity in the

western mountainous regions. Geophysical aspectsof extant cool-season turfgrass will be addressed

for the major species utilized in the United States.Included are the fine-leaf fescues, bluegrasses,bentgrasses, ryegrasses and broad-leaf tall fescue.

Fine-Leaf Fescue.The early species center-of-

origin for fine-leaf fescues (Festucaspecies) hasbeen reported to be in central-Europe during themid-Miocene ~13 mya based on phenotypic andbiogeographical analyses (48). Festucais reportedto be an ancient group and a main evolutionaryline in diversification of the Poeae Tribe (19). Twomain Festucaclades are evident from phenetic andphylogenetic analyses, being fine-leaf and broad-leaf , that had split into diverging lineages (29,31, 93, 94). Within the fine-leaf Festucaclade arosethe F. ovinaand F. rubragroups (94). The latter is

smaller in number of subgroups (69) and is yetto be fully defined due to the paraphyletic nature(2, 6, 10). The F. ovinacomplex is the oldest ofthe turfgrass-types (31), followed in lineage by F.trachyphyllaand F. rubrassp. rubra. Based on phe-netic distance analysis F. ovinaand F. trachyphyllaare distinct, but closely related (2).

Fine-leaf fescues probably diversified in cool,continental, open forest regions, possibly inmountainous areas, and are included in the Festucasubgenus (1, 2, 6, 7). Diversification of the Festuca

genus resulted in a major expansion, with~

400known species (6). Their extant occurrence rangesfrom temperate to alpine to polar regions of bothhemispheres (2). Chewings fescue (F. rubrassp.commutata), hard fescue (F. trachyphylla), sheepfescue (F. ovina), slender-creeping red fescue (F.rubrassp.littoralis), and strong-creeping red fescue(F. rubrassp. rubra)are the fine-leaf Festucaspeciesnow used as turfgrasses in the United States (10,11). These five fine-leaf Festucaare seed propagatedand largely cross-pollinated. The taxonomicclassification of Chewings fescue as traditionally

used is open to question (2). The fine-leaf fescuesmigrated outward throughout much of Europe,into central and eastern temperate Asia (25), andinto Africa. Eventually they moved across theBering Land Bridge into North America and mi-grated southward into Central America and overthe Panamanian Land Bridge into South America(Figure 2). The basic route in the Americas was

3 Personal communication with William A. Meyer of Rutgers University, New Jersey, USA.


13/26


north-to-south via the western mountains ofNorth America to the Andes to Patagonia over aperiod ~3.8 to 10 mya. This migration route hasbeen documented among the Festucaspecies bybiogeographical analyses (48). There also wereoutward migrations into the temperate climaticregions of the continent. These fescues are used

as a turfgrass in the cooler portions of the coolclimatic regions of the United States, being espe-cially adapted to shaded and low-nitrogen fertilityconditions (10, 11).

Most turfgrass-type fine-leaf fescue species(Festuca) are native to North America, havingpersisted for more than three centuries. There areat least 37 Festucaspecies that are native to NorthAmerica (6, 7), including the red, hard, and sheepfescues now used as turfgrasses.

Bluegrass. The early species center-of-originationfor the bluegrasses (Poa) based on phenotypic andcladistic analyses (85) is temperate, open Eurasia.The Poagenus is classified in the Poeaetribe (96),

with diversification being expansive to ~500known species. Global distribution studies revealthe Poaspecies have the highest relative specificdifferentiation in regions of high latitude and highaltitude (47). Poapratensisevolved and diversifiedin geographical regions characterized by a coolcontinental climate and probably in fringe-openmeadow areas interspersed in forests on relatively

fertile soils. Poa trivialisis thought to have evolvedin the cooler, northerly, forest regions of Europeunder relatively wet climatic and soil conditionson clayey soils. The diploid P. trivialisssp. trivi-alishas naturalized in North America (6). Thebluegrass species are propagated by seed and

vegetatively by lateral stems such as rhizomes orstolons.

Poa annuais a ubiquitous, cosmopolitan grass thatis very well adapted to anthropological habitats.It is considered an annual weed in some turfgrass

ecosystems, especially the bunch-type annualbluegrass (P. annuavar. annua). The stoloniferousperennial creeping bluegrass (P. annuavar. reptans)tends to dominate when under a long-term man-aged component in certain turfgrass situations(11). Poa annuais thought to have arisen fromhybridization between P. infirmaand P. supina(6).

A biogeographic migration pattern similar to thefine-leafed fescues through Asia via the Bering

Land Bridge to North America (72) is probable forthe bluegrasses (Figure 2), especially as many Poaspecies have similar temperature responses includ-ing good to excellent freeze stress tolerance (2, 9).Poa pratensishas a circumpolar distribution (85),

with a capability to develop numerous ecotypesto thrive in distinctly different habitats (93).

More than 60 species of Poaare now considerednative to North America (6). Poahas a high spe-cies frequency percentage in regions with a Julymid-summer isotherm below 75 F (24C) (47).Chloroplast-DNA phylogenetics and cladisticanalyses for biogeographical events revealed atleast six groups of Poaspecies had independentlycolonized secondary centers-of-diversification inNorth America, including Kentucky bluegrass andTexas bluegrass. The Poaare found extensively inthe western mountain ranges of North America(41), and the P. pratensiscomplex has been termed

native to the Rocky Mountains (50). The extantKentucky bluegrasses of eastern United Statesmay be of an integrated ancestry with post-glacialreinvasion from the west or south and Europeancolonist introductions (22).

The Poaspecies utilized in the United States asturfgrasses resulting from diversification/migrationinclude Kentucky bluegrass (P. pratensis), roughbluegrass (P. trivialis), and Texas bluegrass (P. arach-nifera) (10, 11). Poa pratensisis a facultative apomicticand highly polyploid. Kentucky bluegrass is widelyused as a turfgrass in the cool climatic regions ofthe United States under minimum shade, whilerough bluegrass is best adapted in moist to wet,shaded conditions in the cooler portions of thecool-humid climatic region (10, 11).

Texas bluegrass is unique among the turfgrass-type Poasin adaptation to warm climates and isnative to the southern Great Plains (85). It is bestadapted to moist, fertile soils and bottom lands.Available evidence suggests P. arachniferaor its an-cestor migrated north from South America, as two

very close sister species occur there (85). Recentlyhybrid cultivars of P. pratensisx P. arachniferahavebeen developed for turfgrass use.

To conclude, a number of Poaspecies are possibleNorth American natives, including P. arachniferaand P. pratensis. Biogeographical analyses/molecularphylogenetic research with a range of Poaspeciessimilar to that for the fine-leaf fescues are needed


14/26


for proper documentation, which should include P.annuaand P. trivialis.

Bentgrass. Based on phenotypic evidence theearly diverged species center-of-origination for thebentgrasses (Agrostisspecies) was in south-centralMediterranean Eurasia (84). The Agrostisgenus is of

ancient origin, and has been morphologically clas-sified in the Poeae, with ~200 known species (6,96, 97) including at least 21 native North Americanspecies. The Agrostisprobably diversified in anenvironment characterized by fringe-forest zonesof partial shade, and minimal moisture stress onpoorly-drained, clayey soils. Mountainous regionsfavored the origination of polyploid forms ofAgrostis(84), with most adapted to narrow habitats(7). Diversification resulted in three bentgrassturfgrasses as now utilized in the United States,including colonial bentgrass (A. capillaris, syn. A.

tenuis), creeping bentgrass (A. stolonifera, syn. A.palustris), and velvet bentgrass (A. canina) (10, 11).

Low levels of interspecific hybridization mayoccur between A. stoloniferaand both A. capillarisand A. castellana, but are not likely for A. canina(13). Allotetraploids A. capillarisand A. stoloniferahave the A

2subgenome in common (49, 85).

Phylogenetic analyses and divergence time esti-mates indicate these two species diverged from acommon ancestor ~2.2 mya (76). Cluster analysisshows the primary cultivated speciesA. capillaris

and A. stoloniferaare more similar to each otherthan the diploid A. caninais to either (4). Agrostisclavatahas been suggested as a progenitor of A.capillarisand A. stoloniferabased on MITE - displaymarker clustering and ploidy prediction (3). Alsogenetic marker studies suggest A. caninamay havecontributed to the evolution of A. stoloniferaas thelikely maternal parent (74). Turfgrass-type Agrostisspecies are propagated primarily by seed, beinglargely cross pollinated. Agrostis stoloniferaalso canbe propagated vegetatively by stolons.

A mountainous migration pattern of Agrostisspe-cies from Europe to North America (72) probablyoccurred similar to that documented for the fine-leaf fescues (Figure 2). The turfgrass-typeAgrostishave good to excellent freeze stress tolerance (9,11). Northern salt marsh and lakeside populationsof A. stoloniferaare considered native to NorthAmerica (6). The species is well adapted to tem-porary flooding and wet soil sites, reflecting the

conditions under which creeping bentgrass origi-nated in Eurasia. The extant bentgrass cultivarstolerate close, frequent mowing while sustaininggood shoot density (10, 11).

The turfgrass-typeAgrostisspecies have beenviewed by some as being introduced to the United

States due to oceanic separation from the earlycenter-of-origination. By inference from recentlyavailable evidence, specifically from the fine-leaffescue research, the turfgrass-type bentgrasses

would be considered possible natives to theUnited States. Hopefully, needed clarifyingbiogeographical analyses/molecular phylogeneticinvestigations will be accomplished.

Ryegrass.The early species center-of-originationfor the ryegrasses (Loliumspecies) based on ge-netic diversity was the open, temperate, southern

Eurasian region along the Mediterranean Sea. TheLoliumgenus is classified in the Poeae (96), withdiversification limited to ~5 known species thatoccurred starting ~2 mya (6, 48). It has been pro-posed that the Loliumgenus and Schedonorus pratensisevolved from a common ancestor (74, 79), and split~2.8 mya (48). Extant Loliumturfgrass cultivarstend to have limited shade adaptation and theircenter-of-origin and diversification probably werecharacterized by open areas.

Propagation is by seed being cross-pollinated,

with most mowed turfgrass cultivars beingbunch-types. The turfgrass-type species used inthe United States include perennial ryegrass (L.perenne) and annual ryegrass (L. multiflorum) (10,11). They are interfertile and naturally intergrade(6). The turfgrass-type perennial ryegrasses areutilized in the warmer portion of the cool climaticregion of the United States and for winter over-seeding of warm-season turfgrasses. They are bestadapted to mild winters and cool-moist summers,and to fertile soils (10, 11).

Migration of the Loliumwas south into northernAfrica, especially in mountainous regions, intonorthern Europe, and also eastward into Asia andIndia (Figure 2). Transcontinental pre-Holocenemigration research is lacking. Lack of freeze stresstolerance (9, 10, 11) may have prevented migrationto North America via the Bering Land Bridge.

Thus, based on the available phenotypic evidencethe ryegrasses utilized for turfgrass purposes


15/26


in the United States are probably naturalizedgrasses first introduced by human trans-Atlanticmovement in the mid-1600s for forage and pas-ture utilization in domestic animal agriculture.Confirmation is needed via biogeographical analy-ses/molecular phylogenetic research.

Tall Fescue.The early species center-of-origination for broad-leaf Schedonoruswas in

mild-temperate Eurasia, separating from fine-leafFestucaduring the Miocene ~15 mya (48, 93). TheSchedonorusgenus is classified in the Schedonorussubgenus (96, 07), with the turfgrass-type beingallopolyploid tall fescue (Schedonorus arundinaceus,syn. Festucaarundinacea) (6). Tall fescue probablydiversified under summers characterized by highertemperatures and less rainfall. S. arundinaceusis

younger in lineage than the turfgrass-type fine-leafFestuca, and based on cluster analysis is closely

related to Schedonorus pratensis(6, 99). Biologicalclock estimates indicate the Asian-American cladeof broad-leaf Schedonorusapparently diverged fromthe fine-leaf Festucaclade ~12 mya (48). Certainhexaploid turfgrass-type tall fescues, such asRebel II and Bonanza, are clustered in a subgroupaccording to cluster analysis (99). Propagation is

by seed being primarily cross-pollinated, with tallfescue behaving as a bunch-type when regularlymowed as a turfgrass.

Migration of S. arundinaceusfrom Europe extendedeastward into Asia and south into Africa, espe-cially via the mountainous regions (Figure 2).

Potential transcontinental migration to the UnitedStates prior to Holocene human activities has notbeen properly investigated. Northward dispersalin Europe may have been limited due to a lack offreeze stress tolerance (9, 10, 11). Tall fescue is bestadapted for turfgrass use in the transitional and

warmer-cool climatic regions of the United Statesunder regular mowing at moderately high heights(10, 11).

Based on the limited available information, tallfescue is considered a naturalized species thought

to have been first introduced into the UnitedStates by transcontinental human activities in themid-1800s for forage and pasture use in domesticanimal production. Biogeographical analyses/molecular phylogenetic research are needed forconfirmation.


16/26


17/26


WARM-SEASON TURFGRASSES

The primitive ancestral center-of-origination forthe warm-season grasses is thought to have beenGondwanan-Africa (28, 72), with West Gondwanamigration to South American and East Gondwanan

migration to India and to Australia via Antarctica.Key synapomorphies include Kranz leaf anatomyand chloridoid bicellular microhairs on the leafepidermis (55). The C

4photosynthetic pathway

characteristic of warm-season grasses evolved inAfrica from C

3ancestral grasses at a later time in

the earths history, and involved multiple bio-chemical and histological C

4events (16, 17, 32, 51,

82). The first evidence of C4photosynthesis in the

Chloridoideae occurred ~33 to 30 mya (15, 17).

Fossil records indicate the ancestral species

of warm-season Poaceae originated in WestGondwana, now Africa, mainly in savanna eco-systems (72). Phylogenetic analyses suggest themonophyletic Panicoideae and Chloridoideaeare derived from the ancestral polyphyleticArundinoideae (32, 52). The PACCMAD cladeexhibited phylogenetic diversifications dur-ing the mid-Miocene through late-Quaternary(16). Phylogenetic molecular studies reveal theChloridoidae may date as early as the late-Oligo-cene ~31 mya (16, 17), but major global migrationmay not have occurred until the Pliocene (67).

Species of C4turfgrass-types tend to have multiplesecondary centers-of-origination in geographicalregions closer to the equator under warm climaticconditions. Twenty-four shifts in phylogeneticdiversification rates have been identified amongthe C

4grass lineages, with 19 during the Miocene

and 5 during the Pliocene (16).

Most warm-season turfgrasses are taxonomicallyclassified within either the Chloridoideae orPanicoideae (96). The Chloridoideae has eighttribes including Cynodonteae and Zoysieae, while

the Panicoideae encompasses two tribes includ-ing the Paniceae. Extant warm-season turfgrassesoccur mostly in the warm, tropical and subtropicalclimates, with an optimum temperature range of80 to 95F (27 to 75C). Most are prone to chillstress in the 52 to 58F (11 to 15C) range, with re-sultant low temperature discoloration and winterdormancy (10, 11, 12). Extant Chloridoideae typi-cally are adapted to survive at mean temperaturesfor the coldest months above 50 F (10 C) (64).

Locations and dating for species centers-of-originand geophysical migrations are increasingly basedon phenotypic, molecular phylogenetic, and alliedcladistic assessments. Fossil types of evidence

are limited as fossilization was restricted in drysavanna climates where warm-season grassesdiversified. Geophysical characteristics of extant

warm-season turfgrasses are addressed for themajor species utilized in the United States, includ-ing bermudagrass, zoysiagrass, St Augustinegrass,centipedegrass, seashore paspalum, carpetgrass,American buffalograss, and gramagrass.

Bermudagrass.The primary center-of-origina-tion for the bermudagrasses (Cynodonspecies) isin open, southeastern Africa (38). Subsequently

early diversification was associated with graz-ing pressure from large herds of herbivorousAfrican, hoofed mammals. Based on biostematicand phylogenetic molecular research, the Cynodonspecies secondary centers-of-origin/diversificationinclude South Africa, India, Afghanistan, China,and Australia (45).

The ubiquitous, cosmopolitan C. dactylonis nowfound throughout the warm-temperate, subtropi-cal, and tropical climatic regions of the world (45).The Cynodongenus is classified in the Cynodonteae

and Chloridinae, with limited diversification of~9 known species and 10 varieties (6, 46, 67, 96).Cluster analysis of DNA amplification productshas confirmed this earlier taxonomic classification.Evidently the genetic diversity of C. dactylonvar.dactylonwas generated internally (45). It thrivesunder soil disturbance on sunny sites. Low-growing Cynodonspecies used as turfgrasses in theUnited States include dactylon bermudagrass (C.dactylonvar. dactylon), a sterile hybrid bermuda-grass (C. dactylonx C. transvaalensis), and a naturalsterile triploid hybrid (Cynodonx magennisii) (10,

11). Molecular phylogenetic analysis has identifiedcluster groups broadly based on relative leaf width(20).

The presumed geophysical migration of theancestral grass was via the East Gondwana landconnection. Subsequent pre-Holocene migration

was outward around Africa, and into southernEurope, Asia, and Australia (Figure 2). Propagationis vegetatively by stolons and rhizomes, and


18/26


by seed for C.dactylonbeing cross-pollinated.The climate under which bermudagrass speciesevolved was subtropical with typically dry sum-mers that resulted in a deep extensive root system,low evapotranspiration rate, extensive lateral stemdevelopment, and superior drought resistance.The modern Cynodonturfgrass cultivars have

retained these water-conserving characteristics,but most lack shade adaptation (10, 11).

Unintended trans-Atlantic human movement ofC. dactylonvia ships of the Spanish conquistadorsprobably occurred in the 1600s to both Northand South America (100), followed by furtherdispersal/naturalization and intraspecies diversifi-cation in the warm climatic regions. The dactylonbermudagrass (C. dactylonvar. dactylon) introducedinto the United States was readily dispersed, andbecame naturalized. The questions are when, by

what means, and if extant native C. dactylonwerealready present in the United States as a result ofearlier natural migration from Africa, possibly viaSouth America. In contrast, African bermudagrass(C. transvaalensis) was probably a human intro-duced species from South Africa to the UnitedStates, with minimal dispersal/naturalization.Biogeographical analyses/molecular phylogeneticresearch are needed to clarify these dispersalaspects.

Zoysiagrass. Phenotypically, the zoysiagrasses

(Zoysiaspecies) are recognized to have a post-ancestral center-of-origin under warm-tropical,open conditions in southeast China. Their primi-tive ancestral grass center-of-origination probablyoccurred in Africa, where it is assumed theysubsequently became extinct during a severe aridperiod (72). The Zoysiagenus is classified in theCynodonteae and Zoysiinae (68), with diversifica-tion being relatively small with ~11 known species(7, 67, 96). Shoots of the turfgrasstype Zoysiaspe-cies possess a high silica content, which suggeststhat herbivorous grazing mammals may not havebeen as significant in their diversification and mi-gration. Based on molecular phylogenetic analysesthe Zoysiagenus arose later than the Cynodon(15).Zoysiaspecies now utilized for turfgrass purposesin the United States include Japanese zoysiagrass(Z. japonica), manila zoysiagrass (Z. matrellavar.matrella), and to a lesser extent mascarene zoysia-grass (Z. pacifica, syn. Z. matrellavar. tenuifolia) (7,10, 11). These three readily intercross suggesting a

close genetic relationship. Also used as a turfgrassis hybrid zoysiagrass (Z. japonicax Z. pacifica)cv. Emerald. Cluster analyses of RAPD revealedgroupings that differ from the classical taxonomicspecies classification (98).

East Gondwana migration of Zoysiaprimitive

ancestors probably occurred from Africa toIndia, although a West Gondwana migration ofthe Zoysiinaeto South America cannot be ruledout entirely without additional investigations(67). Following the separation of India fromAfrica and eventual contact of India with Asia,the Zoysiaancestors migrated to southeast Asia(72). Pre-Holocene migration and secondarycenters-of-origin/diversification for Zoysiaspeciesappear phenotypically to have been limited to theAustralasian region, extending north up into Japanand Korea, south into northeast Australia, and to

the south Pacific Islands extending to Polynesia(Figure 2). The sandy coastal regions and saltmarshes of the southwest Pacific have concentra-tions of Z. matrella, including the Malay peninsula,New Guinea, Philippines, and southeast China(39). Propagation has been primarily vegetativeby rhizomes and stolons, with limited seed avail-ability for Z. japonica. Seed germination amongZoysiaspecies ranges from poor to non-existent,which may have impaired their migration anddiversification.

Zoysiagrasses are used in the United Statesprimarily for turfgrass purposes in the humid-subhumid transitional temperature zone betweenthe cool and warm climatic regions. The Zoysiaspecies diversified in open habitats under atropical climate characterized by hot, humidsummers of southeast China with a large amountof precipitation distributed throughout the year.As a consequence, the zoysiagrasses evolved witha short root system that continues to be expressedin modern turfgrass-type cultivars which con-tributes to a significant reduction in dehydrationavoidance and resultant less drought resistancethan bermudagrass (10, 11). Zoysiagrass cultivarsused as turfgrasses are characterized by a very-slow establishment rate.

Japanese zoysiagrass was present in the UnitedStates by the late-1800s. It probably was inten-tionally introduced by man from southeast Chinaand subsequently has naturalized. Biogeographic


19/26


analyses/molecular phylogenetic research areneeded to clarify the migratory/introduced status.

St Augustinegrass. Evidently the Stenotaphrumgenus is a paleotropic offshoot of Paspalidium(79).The post-ancestral center-of-origination for the StAugustinegrasses (Stenotaphrumspecies), based on

phenotypic diversity, suggests coastal southeasternAfrica since 6 of these 7 known species occur inthat region (79). The extensive occurrence of S.secundatumin the tropical and subtropical Gulf ofMexico Caribbean regions of the Americas sug-gests a secondary center-of-origin/diversification,possibly via the West Gondwanan bridge fromAfrica via South America. The Stenotaphrumgenusis classified in the Paniceae and Setariinae, withdiversification limited to ~7 known species (6,96).

The Stenotaphrumspecies most probably migratedoutward into tropical regions around the primaryand secondary species centers-of-origin/diversi-fication, especially in sandy coastal and streamswale regions (79). Most propagation is vegetativeby stolons, although seed of some genotypes are

viable being cross pollinated while others areself-sterile (79). The inflorescence is adapted forsub-regional island dispersal of seed by ocean cur-rents (79). Transcontinental migration to southeastAsia and northeast Australia probably occurredprior to human movements via the coastal areas

along the Indian Ocean and then southwest viatropical oceanic island hopping (79) (Figure 2).

One species dominates turfgrass usage in theUnited States, that being S. secundatum(10, 11).Floral stigmas and stolon internodes of theFlorida-centered, coarse-textured S. secundatumgroup are purple, while the narrower-leafed Texas-centered Gulf Coast group have yellow stigmasand green stolon internodes (60). The purplestigma types are triploids and tetraploids bothforming seeds that are highly sterile (60). This

would have limited their migration primarily toFlorida. The yellow stigma types are diploids thatform seeds with a reasonable germination capabil-ity and considerable heterozygosity. This allowedselection for improved freeze stress tolerance thatresulted in wider adaptation and migration alongthe Gulf Coast and northward.

The S. secundatumspecies of St Augustinegrass isused for turfgrass purposes in warm tropical and

subtropical southeastern and south-central UnitedStates, extending from Florida to the southerncoastal region of Texas (40). It is best adapted tosandy coastal sites and to moist, well-drained,fertile soils plus a relatively high mowing height(10, 11). The yellow-stigma Gulf Coast Group hasgood shade adaptation, whereas the purple-stigma

group typically has both poor shade adaptationand freeze stress tolerance.

Phenotypic evidence indicates St Augustinegrassis a naturally diversified species, that has becomenative to the United States with two secondarycenters-of-origin/diversification. Biogeographicalanalyses/molecular phylogenetic research areneeded to determine the early intercontinentalmigration routing and timing.

Centipedegrass. An East Gondwanan migration

of the primitive ancestors to the Eremochloaspeciesmay have occurred from Africa to India. Thenfrom India to Asia following the separation ofIndia from Africa and eventual contact with Asia(72). The post-ancestral center-of-origination forcentipedegrass (Eremochloaspecies), based on phe-notypic genetic diversity, is open temperate andsubtropical southeast Asia (40). The Eremochloagenus is classified in the Paniceae and Setariinae,

with diversification limited to ~11 known species(6, 96). E. ophiuroidesis the only species of centipe-degrass now utilized as a low-growing turfgrass

species in the United States (10, 11).

Migration of Eremochloaspecies appears to havebeen outward into tropical southeast and centralChina (44), and to southeast Asia and to Australia(Figure 2). Propagation is by seed being a sexuallyreproducing diploid with some self-incompatibili-ty, and vegetatively by stolons (44).

The Eremochloaspecies evolved in an open tropicalclimate with hot, humid summers and a largeamount of precipitation distributed throughout

much of the year. As a consequence, centipede-grasses evolved with a short root system thatcontinues to be expressed in modern turfgrass-type cultivars (11). Centipedegrass as utilizedfor turfgrass purposes has a very-low nitrogenrequirement (10, 11).

Government records indicate one species of cen-tipedegrass was intentionally introduced into theUnited States in 1916. Whether there were natural


20/26


intercontinental migrations to the Americas beforeHolocene human activities need investigation viabiogeographical analysis/molecular phylogeneticresearch. Until needed research is accomplished E.ophiuroidesshould be considered as introduced intothe United States. It has become naturalized tothe humid and subhumid southeastern and south-

central regions of the United States (40).

Seashore Paspalum. The primitive ancestralcenter-of-origination for the Paspalumsis thoughtto be West Gondwana-African, with migration toSouth America prior to continental plate separa-tion of Pangea. Thus, South America was a keycenter-of-origin, typically in brackish areas andsalt marshes. However, the species center-of-origin for certain fine-leaf turfgrass-type Paspalumspecies based on phenotypic evidence is tropicaland subtropical southern Africa, with subsequent

secondary diversification centers in coastal SouthAmerica and southeastern North America, basedon phylogenetic molecular research and clusteranalysis (59). The Paspalumgenus is classified inthe Paniceae and Setariine, with ~320 knownspecies (6, 96) with seven cluster groups identified(59). There are very-coarse, intermediate, and fine-leaf species and ecotypes. The fine-leaf P. vaginatumis the only species group utilized as a turfgrass inthe United States (36).

Pre-Holocene migration of the fine-leaf P. vaginatum

expanded primarily around the tropical andsubtropical coastal and stream swales of southernAfrica, that were characterized by brackish, marshecosystems including tidal flooding (Figure 2).Propagation is vegetative via rhizomes and stolons,and also can be by seed being a diploid with crosspollination and considerable self-sterility (21). It ismost valuable as a turfgrass on soils with high saltlevels.

Early introduction of fine-leaf P. vaginatuminto theUnited States probably was by human activity via

ships to southeastern Atlantic coastal ports duringthe 1700s (36), as well as into the coastal West

Indies. This ecotype has become a naturalizedspecies, persisting primarily in the brackish, sandycoastal regions of southeastern and south-centralUnited States.

Carpetgrass. A post-ancestral, distinct second-ary center-of-origin for the carpetgrasses (Axonopus

species) is phenotypically considered to have beentropical Brazil and extending into the Caribbeanregion of the Americas (14, 40, 67). Their primitiveancestral grass and related geophysical aspectsmay have involved origination in Africa andmigration to east and central Brazil in SouthAmerica (14). The Axonopusgenus is classifiedin the Paniceae and Setariine, with significantdiversification indicated by ~100 species (6). Thetwo low-growing, turfgrass-type species in use arecommon carpetgrass (A. fissifolius, syn. A. affinis),and tropical or broadleaf carpetgrass (A. compressus)

(10, 11). They prefer open sites and wet soils thatare periodically flooded.

Pre-Holocene migration of Axonopusspecies pre-sumably was outward regionally from the Africanancestral center-of-origination, and then fromsecondary centers-of-origin in South America,and eventually southeast Asia, and southeasternUnited States (67) (Figure 2). Propagation is

vegetatively by stolons and by seed being a diploidwith cross pollination and some self-sterility (21).Phenotypic observations reveal a wide-spread,

extant global distribution in the tropical-subtropical climatic regions of the Americas,Southeast Asia-Pacific Islands, and Africa. In termsof turfgrass use, common carpetgrass is found inthe southeastern United States with limited use,

while tropical carpetgrass is widely used in south-east Asia. Common carpetgrass is best adapted toacidic, moist to wet soils (10, 11).

Carpetgrass is native to the southeastern UnitedStates and the American tropics and subtrop-ics (6, 41). Biogeographical analyses/molecular

phylogenetic research would elucidate the earlydiversification and migration of carpetgrass.


21/26


22/26


The three grass species have been utilized asturfgrasses primarily under unirrigated conditionsin the Great Plains region of the United States (10,11). They are best adapted to semi-arid climates

where the precipitation is not sufficient to sup-port most tree and shrub species (10, 11). Theytend to become dormant during extensive sum-

mer droughts, their drought survival is achievedprimarily by a dormancy escape mechanism, ratherthan an inherent dehydration tolerance componentof drought resistance. These semi-arid, warm-season grasses have a relatively moderate shootdensity.

Perennial turfgrasses with a higher water require-ment are less favored in unirrigated, semi-arid

environments of the Great Plains. However, thehigh density, more aggressive turfgrass species,such as Kentucky bluegrass and bermudagrass,tend to dominate these three species in higherprecipitation regions (10, 11). Also, the semi-aridenvironments in which these genera evolvedresulted in genotypes that were not subjected to

pathogen pressures common to humid regions andconsequently did not result in strong selection forresistance to such diseases.

American buffalograss and blue and side-oatsgramagrasses were originally naturalized speciesto the United States, that also may be termednative species.

SUMMARY COMMENTSCertain groups advocate that only plants andgrasses native to a particular region should begrown in that landscape. A premise for this con-cept is that native grasses have superior adaptationcompared to any introduced, naturalized grasses.There are naturalized grasses as well adapted oreven better adapted to certain climatic-soil regionsof the world than the native grasses. Actuallyneither category is genetically stable, rather theycontinue to diversify.

The term native has been used as an arbitrary con-cept to access whether a species belongs naturallyat a specific site. However, it is a questionableapproach to separate a natural process from thepresence and influence of human activity. While it

is appropriate and fortunate that some individu-als are interested in preserving and propagatingnative grass stands in various climatic regions, it isunwise and even detrimental to promote laws orother means that force all individuals to use onlynative grasses in landscape plantings throughouta city or region. Advocating only the use of nativeplants in what is essentially an artificial non-native environment of urban structures, concrete,asphalt, and disturbed lands is not logical. Manyplants arbitrarily identified as native to a localnatural environment may not be adapted to anearby urban ecosystem, while certain natural-ized plant species may be better adapted andmore capable of enhancing the functional humanquality-of-life in urban areas.


23/26


REFERENCES:1. Aiken, S.G., M.J. Dallwitz, C.L. McJannet, and

L.L. Consaul. 1996 onwards. Festucaof NorthAmerica: descriptions, illustrations, identificationand information retrieval. http://delta-intkey.com/festuca.

2. Aiken, S.G., M.J. Dallwitz, C.L. McJannet, and L.L.Consaul. 1997. Biodiversity among Festuca(Poaceae)in North America: diagnostic evidence from DELTAand clustering programs, and an INTKEY packagefor interactive, illustrated identification andinformation retrieval. Canadian Journal of Botany.75:1527-1555.

3. Amundsen, K.L. 2009. Origin and evolution ofcultivated Agrostisspp. PhD dissertation, GeorgeMason University, Fairfax, Virginia, USA. 144 pages.

4. Amundsen, K. and S. Warnke. 2011. Speciesrelationships in the genus Agrostisbased on flowcytometry and MITE-display molecular markers.

Crop Science. 51:1224-1231.5. Axelrod, D.I. 1985. Rise of the grassland biome,

central North America. The Botanical Review.5(2):163-201.

6. Barkworth, M.E., K.M. Capels, S.Long, and M.B.Piep (coeditors). 2003. Flora of North America,Magnoliophyta: Commelinidae (in part): Poaceae.Oxford University Press, New York City, New York,USA. 25 (part 2): 809 pp.

7. Barkworth, M.E., L.K. Anderton, K.M. Capels, S.Long , and M.B. Piep (coeditors). 2007. Manualof Grasses for North America. Intermountain

Herbarium and Utah State University Press Logan,Utah, USA. 630 pp.

8. Barnard, C. and O.H. Frankel. 1964. Grass, grazinganimals, and man in historic perspective. (InGrasses & Grasslands, ed. C. Barnard). Macmillan& Company Ltd., London, UK. p. 1-12.

9. Beard, J.B. 1966. Direct low temperature injuryof nineteen turfgrasses. Quarterly Bulletin ofthe Michigan Agricultural Experiment Station.48(3):377-383.

10. Beard, J. B. 1973. Turfgrass: Science and Culture.Prentice-Hall, Inc., Englewood Cliffs, New Jersey,

USA. 658 pp.11. Beard, J.B and H.J. Beard. 2005. Beards Turfgrass

Encyclopedia for Golf Courses, Grounds, Lawns,Sports Fields. Michigan State University Press, EastLansing, Michigan, USA. 513 pp.

12. Beard, J. B and P. O. Cookingham. 2007. WilliamJ. Beal Pioneer applied botanical scientistand research society builder. Agronomy Journal.99:1180-1187.

13. Belanger, F.C., T.R. Meagher, P.R. Day, K. Plumley,and W.A. Meyer. 2003. Interspecific hybridization

between Agrostis stoloniferaand related Agrostisunderfield conditions. Crop Science. 43:240-246.

14. Black, G.A. 1963. Grasses of the genus Axonopus, ataxonomic treatment. Advancing Frontiers of PlantScience. 5:1-186.

15. Bouchenak-Khelladi, Y., N. Salamin, V. Savolainen,F. Forest, M. van der Bank, M.W. Chase, and T.R.Hodkinson. 2008. Large multi-gene phylogenetictrees of the grasses (Poaceae): progress towardscomplete tribal and generic level sampling.Molecular Phylogenetics and Evolution. 47:488-505.

16. Bouchenak-Khelladi, Y., G. A. Verboom, T. R.Hodkinson, N. Salamin, O. Francois, G. N.Chonghaile, and V. Savolainen. 2009. The originsand diversification of C grasses and savannaadapted ungulates. Global Change Biology. 15:2397-2417.

17. Bouchenak-Khelladi, Y., G.A. Verboom,V. Savalainen, and T.R. Hodkinson. 2010.Biogeography of the grasses (Poaceae): aphylogenetic approach to reveal evolutionary historyin geographical space and geological time. Botanical

Journal of the Linnean Society. 162:543-557.

18. Burkart, A. 1975. Evolution of grasses andgrasslands in South America. Taxon. 24(1):53-66.

19. Burton, G.W. and J.S. Andrews. 1948. Recovery andviability of seed of certain southern grasses andlespedezas passed through the Bovine digestivetract. Journal of Agricultural Research. 76:95-103.

20. Caetano-Anolls, G., L.M. Callahan, P.E.

Williams, K.R. Weaver, and P.M. Gresshoff. 1995.DNA amplification fingerprinting analysis ofbermudagrass (Cynodon): genetic relationshipsbetween species and interspecific crosses.Theoretical Applied Genetics. 91:228-235.

21. Carpenter, J.A. 1958. Production and use of seedin sea-shore paspalum. Journal of the AustralianInstitute of Agricultural Science. 24:252-256.

22. Carrier, L. and K.S. Bort. 1916. The history ofKentucky bluegrass and white clover in theUnited States. Journal of the American Society ofAgronomy. 8(4):256-266.

23. Cerling, T.E., Y. Wang, and J. Quade. 1993.Expansion of C

4ecosystems as an indicator of

global ecological change in the late Miocene.Nature. 361:344-345.

24. Chapman, G.P. 1996. The Biology of Grasses. CABInternational, Wallingford, Oxon, UK. 273 pp.

25. Chen, X., S.G. Aiken, M.J. Dallwitz, and P.Bouchard. 2003. Systematic studies of Festuca(Poaceae) occurring in China compared with taxain North America. Canadian Journal of Botany.81:1008-1028.


24/26


26. Clark, L.G., W. Zhang, and J. F. Wendel. 1995. Aphylogeny of the grass family (Poaceae) based onndhFsequence data. Systematic Botany. 20(4):436-460.

27. Clayton, W.D. 1975. Chorology of the genera ofGramineae. Kew Bulletin. 30:111-132.

28. Clayton, W.D. 1981. Evolution and distribution ofgrasses. Annals of the Missouri Botanical Garden.68:5-14.

29. Clayton, W.D., R. Cerros-Tlatilpa, M.S. Kinney,M.E. Siqueiros-Delgado, H.L. Bell, M.P. Griffith,and N.F. Refulio-Rodiguez. 2007. Phylogenetics ofChloridoideae (Gramineae): a preliminary studybased on nuclear ribosomal internal transcribedspacer and chloroplast trnL-F sequences. (InMonocots: Comparative Biology and EvolutionPoales, eds. J.T. Columbus, E.A. Fariar, J.M. Porter,L.M. Prince and M.G. Simpson). Rancho Santa AnaBotanic Garden, Claremont, California, USA. pp.565-579.

30. Crepet, W.L. and G. D. Feldman. 1991. The earliestremains of grasses in the fossil record. American

Journal of Botany. 8:1010-1014.

31. Darbyshire, S.J. and S.I. Warwick. 1992. Phylogenyof North American Festuca(Poaceae) and relatedgenera using chloroplast DNA restriction site

variation. Canadian Journal of Botany. 70:2415-2429.

32. Davis, J.I. and R.J. Soreng. 1993. Phylogeneticstructure in the grass family (Poaceae), asdetermined from chloroplast DNA restriction site

variation. American Journal of Botany. 80:1444-1454.

33. Delcourt, P.A., H.R. Delcourt, C.R. Ison, W.E.

Sharp, and K.J. Gremillion. 1998. Prehistoric humanuse of fire, the eastern agricultural complex, andAppalachian oak-chestnut forests: paleoecology ofCliff Palace Pond, Kentucky. American Antiquity.63(2):263-278.

34. Dore, W.G. and L.C. Raymond. 1942. PastureStudies XXIV. Viable seeds in pasture soil andmanure. Scientific Agriculture. 23(2):69-79.

35. Doyle, J.J., J.I. Davis, R.J. Soreng, D. Garvin, andM.J. Anderson. 1992. Chloroplast DNA inversionsand the origin of the grass family (Poaceae).Proceedings of the National Academy of Sciences.

USA. 89:7722-7726.36. Duncan, R.R. and R.N. Carrow. 2000. SeashorePaspalum The Environmental Turfgrass. Ann ArborPress, Chelsea, Michigan, USA. 281 pp.

37. Ehleringer, J.R., R.F. Sage, L.B. Flanagan, and R.W.Pearcy. 1991. Climate change and the evolution ofC

4photosynthesis. Trends Ecological Evolution

6(3):95-99.

38. Forbes, I., Jr. and G.W. Burton. 1963. Chromosomenumbers and meiosis in some Cynodonspecies andhybrids. Crop Science. 3:75-79.

39. Goudswaard, P.C. 1980. The genus Zoysia(Gramineae) in Malesia. Blumea 26:169-175.

40. Gould, F. W. 1975. The Grasses of Texas. TexasA&M University Press, College Station, Texas,USA. 653 pp.

41. Gould, F.W. and R.B. Shaw. 1983. Grass Systematics.Texas A&M University Press, College Station,Texas, USA. 397 pp.

42. Grass Phylogeny Working Group. 2000. A phylogenyof the grass family (Poaceae) as inferred fromeight character sets. (In Grasses: systematics andevolution. S.W.L. Jacobs and J.E. Everett). CSIRO,Melbourne, Australia. p. 3-7.

43. Grass Phylogeny Working Group. 2001. Phylogenyand subfamilial classification of the grasses(Poaceae). Annals of the Missouri BotanicalGarden. 88(3):373-457.

44. Hanna, W.W. and G.W. Burton. 1978. Cytology,reproductive behavior, and fertility characteristicsof centipedegrass. Crop Science. 18:835-837.

45. Harlan, J.R. and J.M.J. de Wet. 1969. Sources ofvariation in Cynodon dactylon(L.) Pers. Crop Science.9:774-778.

46. Harlan, J.R., J.M.J. de Wet, K.M. Rawal, M.R.Felder, and W.L. Richardson. 1970. Cytogeneticstudies in CynodonL.C. Rich. (Gramineae). CropScience. 10:288-291.

47. Hartley, W. 1961. Studies on the origin, evolution,and distribution of the Gramineae. IV. The genusPoa L. Australian Journal of Botany. 9:152-161.

48. Inda, L.A., J.G. Segarra-Moragues, J. Mller, P. M.Peterson, and P. Cataln. 2008. Dated historical

biogeography of the temperate Loliinae (Poaceae,Pooideae) grasses in the northern and southernhemispheres. Molecular Phylogenetics andEvolution. 46:932-957.

49. Jones, K. 1956. Species differentiation inAgrostis.Part II. The significance of chromosome pairingin the tetraploid hybrids of Agrostis caninasubsp.MontanaHartmn., A. tenuisSibth. and A. stoloniferaL.

Journal of Genetics. 54:377-393.

50. Keck, D.D. 1965. Poa. (InCalifornia Flora, A. Munz).University of California Press, Berkeley, California,USA. p. 1482-1490.

51. Kellogg, E. A. 2000. The grasses: A case study inmacroevolution. Annual Review of Ecology andSystematics. 31:217-238.

52. Kellogg, E.A. and C.S. Campbell. 1987. Phylogeneticanalyses of the Gramineae. (InGrass Systematicsand Evolution. ed. T.R. Soderstron, K.W. Hilu, C.S.Campbell and M.E. Barkworth). Smithsonian Inst.Press, Washington, D.C., USA. pp. 310-322.

53. Kendle, A.D. and J.E. Rose. 2000. The aliens havelanded! What are the justifications for native only


25/26


policies in landscape plantings? Landscape andUrban Planning. 47:19-31.

54. Kingston, J.D., B.D. Marino, and A. Hill.1994. Isotopic evidence for Neogene hominidpaleoenvironments in the Kenya Rift Valley.Science. 264:955-959.

55. Krans, J.V., J.B Beard, and J.F. Wilkinson. 1979.Classification of C

3

and C4

turfgrass species basedon CO

2compensation concentration and leaf

anatomy. HortScience. 14:183-185.

56. Latorre, C., J. Quade, and W.C. McIntosh. 1997.The expansion of C

4grasses and global change in

the late Miocene: Stable isotope evidence from theAmericas. Earth and Planetary Science Letters.146:83-96.

57. Levin, D.A. 2001. The recurrent origin of plant racesand species. Systemic Botany. 26(2):197-204.

58. Linder, H.P. 1987. The evolutionary history of thePoales/Restionales a hypothesis. Kew Bulletin.42(2):297-318.

59. Liu, Z.W., R.L. Jarret, R.R. Duncan, and S.Kresovich. 1994. Genetic relationships and variationamong ecotypes of seashore paspalum (PaspalumvaginatumSwartz) determined by random amplifiedpolymorphic DNA (RAPD) markers. Genome.37:1011-1017

60. Long, J.A. and E.C. Bashaw. 1961.Microsporogenesis and chromosome numbers in St.Augustinegrass. Crop Science. 1:41-43.

61. MacFadden, B.J. 2000. Origin and evolution of thegrazing guild in Cenozoic New World terrestrialmammals. (InEvolution of herbivory in terrestrial

vertebrates: perspectives from the fossil record. ed.H. Sues). Cambridge University Press, Cambridge,England, UK. pp. 223-244.

62. Mathews, S., R.C. Tsai, and E. Kellogg. Phylogeneticstructure in the grass family (Poaceae): evidencefrom the nuclear gene phytochrome B. American

Journal of Botany. 87:96-107.

63. Matthes, C.A. and S.K. Davis. 2001. Molecularinsights into the evolution of the Family Bovidae:A nuclear DNA perspective. Molecular Biology andEvolution. 18(7):1220-1230.

64. Muller, J. 1981. Fossil pollen records of extant

angiosperms. The Botanical Review. 47:1-140.65. Neto, M.S., R.M. Jones, and D. Ratcliff. 1987.

Recover of pasture seed ingested by ruminants.1. Seed of six tropical pasture species fed tocattle, sheep and goats. Australian Journal ofExperimental Agriculture. 27:237-246.

66. Ortmann, J., W.H. Schacht, and J. Stubberndieck.1998. The Foliage is the Fruit hypothesis: complexadaptations in buffalograss (Buchloe dactyloides).America Midland Naturalist. 140(2):252-263.

67. Peterson, P. M., J. T. Columbus, and S. J. Pennington.2007. Classification and biogeography of new worldgrasses: Chloridoideae. Aliso. 23:580-594.

68. Peterson, P.M., K. Romaschenko, and G. Johnson.2010. A classification of the Chloridoideae(Poaceae) based on multi-gene phylogenetic trees.Molecular Phylogenetics and Evolution. 55:580-598.

69. Piper, C.V. 1906. North American species of Festuca.Contribution from the U.S. National Herbarium,Washington, D.C. 10:1-48.

70. Prasad, V., C. A.E. Strmberg, H. Alimohammadian,and A. Sahni. 2005. Dinosaur coprolites and theearly evolution of grasses and grazers. Science.310:1177-1180.

71. Quinn, J.A., D.P. Mowrey, S.M. Emanuele, andR.D.B. Whalley. 1994. The Foliage is the Fruithypothesis: Buchloe dactyloides(Poaceae) and theshortgrass prairie of North America. American

Journal of Botany. 81(12):1545-1554.

72. Raven, P.H. and D.I. Axelrod. 1974. Angiosperm

biogeography and past continental movements.Annals of the Missouri Botanical Garden. 61:539-673.

73. Rezaei, H.R., S. Naderi, I.C. Chintauan-Marquier,P. Taberlet, A.T. Virk, H.R. Naghash, D. Rioux, M.Koboli, and F. Pompanon. 2010. Evolution andtaxonomy of the wild species of the genus Ovis(Mammalia, Artiodactyla, Bovidae). MolecularPhylogenetics and Evolution. 54:315-326.

74. Rotter, D., K.V. Ambrose, and F.C. Belanger. 2010.Velvet bentgrass (Agrostis caninaL.) is the likelyancestral diploid maternal parent of allotetraploidcreeping bentgrass (Agrostis stolonifera L.). Genetic

Resource Crop Evolution. 57:1065-1077.75. Rotter, D., K. Amundsen, S.A. Bonos, W.A. Meyer,

S.E. Warnke, and F.C. Belanger. 2009. Moleculargenetic linkage map for allotetraploid colonialbentgrass. Crop Science. 49:1609-1619.

76. Rotter, D., A.K. Bharti, H.M. Li, C. Luo, S.A. Bonos,S. Bughrara, G. Jung, J. Messing, W.A. Meyer,S. Rudd, S.E. Warnke, and F.C. Belanger. 2007.Analysis of EST sequences suggests recent originof allotetraploid colonial and creeping bentgrass.Molecular Genetics and Genomics. 278:197-209.

77. Sanchez-Ken, J.G., L.G. Clark, E.A. Kellogg, and

E.E. Kay. 2007. Reinstatement and emendation ofsubfamily Micrairoideae (Poaceae). SystematicBotany. 32:71-80.

78. Sandve, S.R. and S. Fiellheim. 2010. Did gene familyexpansions during the Eocene-Oligocene boundaryclimate cooling play a role in Pooideae adaptationto cool climates? Molecular Ecology. 19:2075-2088.

79. Sauer, J.D. 1972. Revision of Stenotaphrum(Gramineae: Paniceae) with attention to itshistorical geography. Brittonia. 24:202-222.


26/26

80. Scharf, E. 2010. Archaeology, land use, pollen andrestoration in the Yazoo Basin. Veget. HistoryArchaeobotany. 19:159-175.

81. Scholz, H.1975. Grassland evolution in Europe.Taxon. 24(1):81-90.

82. Sinha, N.R. and E.A. Kellogg.1996. Parallelism anddiversity in multiple origins of C

4photosynthesis in

grasses. American Journal of Botany. 83:1458-70.

83. Smith, A.G., J.C. Briden, and G.E. Drewry. 1973.Phanerozoic world maps. (InOrganisms andContinents through Time. ed. N.F. Hughes.)Palacontol. Assian. London, Special PaperPalacontol. 12:1-43.

84. Sokolovskaya, A.P. 1938. A caryo-geographical studyof the genus

Turgrass Report

Documents

Transcript of Turgrass Report