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Non-flying mammals as pollinators
he notion? that non-flying mammals might pollinate flowers was first proposed over 50 years ago by . Since then there have
ofthe species
under consideration are small, nocttlrnal and cryptic, necessitating the development of new techniques7J (Table 1, Many
Fig.
1). Other
species
rkr~ lal-ger.
flowers
non-destructively
com-
(Table 2). It is likely that there are still more species involved, particularly among ~0ct~rna~ mammals from places such as the neotropics and Asia, which have been relatively poorly studie Many plant species are involved in these interactions. VisitatiOi1 t0 flowers Of m0re than 85 species from 43 genera and 19 families has so far been documented (Table 3). The interaction appears to be particul lent in Australia, where visit a range of shrubs and trees from at least 59 species. Particular preference is shown for members
S.M. Carthew is at the Dept of Envlronmentai Science and Management. University of Adelaide, Roseworthy Campus, Roseworthy. South Australia, 5371 Australia; R.L. Goldmgay is at the School of Resource Science and Management, Southern Cross Univrrslty. PO Box 157 L~siiiorr. NSW 2480 bs;4ia”
ties are visited) and Myrfaceae (notably ~~c~ly~~~.~ of which at least 18 species are many other areas, a species is serviced b r example, in the neogenus ~ua~Q~i~~~ is visited by 12 species of
but are
found in more-remote areas that have not been well studied There have been a numbea until now’l. Recent studies in this of attempts to synthesize inforfield have focaisctl ~~~~~~~~~r~ly on 111Isuring the c~ffWti\~.Wt’ss rMion about the irlteraction between some groups of nonof these animals as pollinators. an three main types of data ale and the fiowers they visitr-4,1!‘. have been sought (Table 1). First, animals must be observed to visit flowers Second, rhey mu srantial loads of n and transport them to the flowers of a lack of c0rn~e~~~ion wi conspecific plants. nid, evidence is required to show that Australia, at least, ail m Ily pollinate flowers. and that such ~o~~~~ati0~~s
ted that a variety of mammals visited flowers across three continents; namely Australia, Africa ai”-!?. More recent stodiesl:i-lli have exer of species and have shown that it is even more comlinon and widespread than was first thought. There are now ~~e~~-~~c~I~entec~cases of ~~~~-f~yi~i~mammai ~o~~~~~at~0~~ ~~v[~~v~~~~ at Ieast 5y t~~~~~~~~ among 19 families and six ~?es~-~eprese~te~~groups are the ma *e 12 species, and the primate a. of which there are ni iie flower visitation by studied less often than for marsupials (I.5 versus 24 studies, not ~~c~ud~~ganecdotal accaunrs). there aDnear tn_ 170 m-r+ __.A.“.L species uf primates involved in pofl~nat~o~than any other ,OroW: 28 species of primates have been observed visiting
e 2). and at least some of visited by birds?. Other r indicates that ~~ecta~-~eedi~gbats may be Pp_esent with nonflying rnarnrna~s~:~~~4.~~~. TFhere have also been conflicting ideas about the imp0rtnnce of the interaction. For example, it is sometimes thought of as irncidental, with animals only visiliing flowers irrqplarlyl;. A~te~~~t~ve~y~plants may be visited by am array of gPoslinators”“,“,“, several of whi may be equally effective in p~~l~~at~~g~.For some plants mds may well act as the sole p particularly likeelyfor some of the plmts visited by lermrs in ~adagas~a~~~~,~4.~~ may be that these mamnaiian y~dlinators have shared a long utionary with the piants that ihcy visat, and that relation tes back to the Cretaceous3v4J4. However, this does not necessarily mean that the rehtionsbip is co-evolved.
Observations of flower visiting for nectar or pollen do not confirm that an animal is an effective pollinator. Data are required to demonstrate po?len transfer by mammaLs (Table 1). There are several ways this information can be obtained. Pollen can often be seen on the fur of foraging animals, since they typically get pollen all over their bead and bodyiJl,?‘l. Analysis of faecal samples further indicates that animals often ingest pollen during ctar feeding’“. This may incidental, or it may refl active feeding on polien6J4 or even regular grooming following nectar feeding”. Alternatively, pollen loads can be measured on captured animal r immediately after e or nder during foraging ntrolled conditions (Box 1). ates of pollen removal from
tWniber of studies Type of evidence
Il1ett,oc
Regular flower wsltatton
Direct obsen?at!ori Direct obscr;at;or,
Non-destructive Importance
Successful
feeding
of nectar and/or
pollen In diet
removal of pollen from flowers
Transportabon
of pollen 0’1 fur
P:e 1990
Post 1990
ir;ld
:3
~pt,~,i:
Trapping near flowers Remote cameras TracC+a 0
1 2 0 1
11 1 3 1 1
Direct observation Direct observation
- wld - captive
5 1
8 1
TImed obsenatlons Faecal analysis I>:etary requlrelments
wild
5
5
i
2
1
0
Pollen removal experiments
1
3
Dtrect observation Direct observatron
3 0 8
7 3 2
wild captlbe
Pollen loads Successful contact of sttgmas
Direct observabon
-wild
2
2
Movement between plants (showing ablkty to cross polilrlateI
Direct observabon Trackings’
-wild
6 1
6
Rdellty to a species
Direct observation I rddmg
1
0
Successful
pollmahon
Pollen germination
Successful
reproduction
Selective
3Tracktng includes the use of radiotracking,
nd compared with rates for OdS more acti~e~~.~. These tee WS t non-flying mammals pick up and carry large amounts of pollen, and are at least as good as other pollinators such as tive ~ol~~~ato~sthey must not ody must also deposit it ween conspecihic plants knowledge of the foraging behaviour of potentia ortant, as it will determine patterns of pollen flow are
spool-and-line
w~lrJ
1
0
1
experiments
0
2
seed set expenments
1
2
trackmg and fluorescen!
powder tracking
single tree for some time and empty systematically all flowers of nectar. However, species that a are most likely to efft *+self pollination. ecies occur in troops or family groups, and these may make regular inter-plant movements, dte~
tating cross-~oll~nat~o~l.
wav in which non f!ykg msmm~k fxage within and between
e of inter etween plants, and di
tances apart. For those smaller, less-mobile nectarivorous mammals, it may be advantageous to remain in a
g. 1. A waratah inflorescence (Telopea speciosissima) being visited by an eastern pygmy possum (Cercartetus nanus). The photograph was taken in the field usmg automated photography. The next photograph in the sequence showed ihe animal with its head buried in the back inflorescence.
l-able 2. .~ .~~ ~~ No. species
Otdt‘r
Family
hla:supidiik
Petauridae [Aust “1 iiasyt~tldae @St.; Eurramyldae (Ausr i
‘I i
Tarslpldidae Didelphldae 9,
1 2 3
5 :
&-ro~.‘,+m 1*a*c‘t . . L.L,-.“.’ (Aust.] (CA) (SAI
1 4. 1” 1 2
Rodentia
Mundae
(Aus1.i tSAfr.1 Gliric’ae (CAfr.1 Cricetldae $.?.I
Primates
CfArcopithecldae (CAfr l.orlsldae (CAfr.1 Galagidae [CAfr.) Ikmur~dar (Mad I C,ilIl:llrllltl,~c’ ,i.#\i II ISA! Cr~irlx! (CA1 ” is.4
II
1
+ 1 1 6, .3’ I” 5” 3 1, 4
Scandt~ntl~~
1tl&II!liCiU iG”fll
1
Carnlvold
V~verriilx(Ci\bI
Plocva~l’:lcle (C4’!
1 2
Macrosceklea
Macroscelldldae
1
Aust.. Austrak:
CA, Central America: SA. South America; SAfr.. South Alrica: CAfr.. GSI. Greater Sunda islands diurnal species. all other species are nocturnal.
CentralAfrica: Mad.. Madagascar: “Indicates
(Skft.)
rroteaccae Myriaceae Rul acoalr S~iplnd.W<.lc h
showing traulininti behaviour !s. In some instances, araimals may n&e qbite long distances between visits, avoiding near neighbours, for presumably more rewarding plants. Species that visit a few flowers on a plant in quick succession and carry pollen over long distances are likely to effect crosspollination and promote more long-distance gene flow. Flower visitors may also vary their behaviour during a flowering season. For example, in one study on the gliding mars3pial (Pelu~r~ austr~lis), Goldingay?” found that when [lowers were scarce, animals were forced to make longdistence movements (often more than 50 m) between trees, but tended to stay in a single tree for long periods. Conversely, when flowers were abundant, animals spent ler,s time in individual trees but moved between ~eig~bo~~;~g trees. This indicates that pollen flow may vary throu# a season, and thus have imporlant imphcations for gene exchange, particularlly in those @ants that are self-compatible.
nammals Bead to the production of seed? IT1 sonW instanr-s it Cilll be ~kssuY71cc~ that non-Ilying n~ammais are ~o~~~~at~ng effectively because of the morphological fit between pollinator and flower (e.g. POi SOI1K” Bemursz:~). However, it is difficult to conduct experiments that show conclusively that non-flying mammals are capable of effective pollination. or that they are ‘better’ pollinators than other visitors. This requires a comparison of the proportional co~tr~bnt~o~ ~f~o~~-~~y~~g mammals to pollination with that for all other flower visitors. Selective exclusion experiments can be conducted, whereby non-flying maminals are rxcludetl from visiting flowers that all other pollinators can access. To date, the method has been used on only a few species of the Proteaceae. dunksi~ spr’nuloso ar:d B. j~te~~~~~li~ hnm Australia”-7 and Proreu a~n~~~x~call~isand P ~?ur~~~~l~~~~ from South Africaz!‘. For R. spinuloscr.experiments revealed that marsupials are at least equally as effective as birds at jri~llill;itiug firw~~rs. ;tnd at litales Iuay be better than their avian coePnterparts’i.T.Wiens et al.‘!‘showed that fruit set on ii r&t 4 Pr’1.01~ was reduced by up to 5fPX, on ina’lorescences whcrc manmnai visitation was excluded. The reason that so frw attempts have been: made to assess the effectiveness of il~iU~Il)~illi~llp~SlilI~~tOlSis tllat tllc PlalIP SpCckS invOlvct8 often exhibit low levels of natural fruit set or have flowers that are inaccessible or difficult to cage (e.g. mass-flowering trees).
bhXOSacede Cappandaceae Combretacede
Bombacaceae Euphorblaceae Guttlferae Musaceae Acanthaceae Cilrvsobalanaceae
(timing of flower opening. pollen ~~~~se~~tati~)~ and nectar secretion) hail traits as adaptations to ~o~l~~~at~~~~~ by ~~~)~~~f~y~~~g mammals (Box 2). For example. flowers are often large and robust IS.23 (to cope with large and sometimes vigorous feeders), or presented as multi-flowered inflorescenc&.l1.~1-2:{. iBecame many non-flying mammals are ljocturnal and iPilW acute olfactory senses, flowers are often drab in colku~tii:& :,‘L .l.mib~~ Of poiien glalils sdliipied frOrl1 the lied& of fiord1 vlsltors has been used Lo d~sebs bl!Js dn\l no11QLn”‘~‘~~? “I, but exude a punflying mammal5 for their llotent~al as pollmators~~. Such studies report birds with pollen loads of several thousand gralns and gent odo~r~~~~l. To provide a mammals ~th Pollen loads of a few hundred grams. However. these samgles are scarcely comparable because mammals were sampled aiIer remaining m traps overnight, while bards were sampled soon after capture In mist net+. Morepredictable and worthwhile Precise assessment Of pollen loads has involved sampling pollen from mammals trapped at l-3 ii Intervals and also after resource for mammals, piants hand capture’. .“. ComParlSon with mammals sampled after about Xh in haps showed that pollen loads decreased draoften flower profusely and mdtlca@ Ihe lorlrSer mammalsstayedIntraps. indlcatmg removal during groomingz’. Sampling oftwo marsupiais ~Ankci,:produce copious amounts flus stuart~~ and Waurus brevicepslwithln 1 h of capture has revealed total pollen loads of 3000-15 000 pollen grains of sugar-rich ~e~f~~l4.1W.2~3~ Per bead’. This value suggests conslderable potential to effect pollmatton. They should comparatively
also produce large amounts
of poller~~‘~,because
mam are often larger than other pollinators (which may red precision in pollen delivery and transfer] and- some s ies include @ilen in their dieP. Despite these generatizations, there can be no allencompassing ‘non-flying mammal pollination syndrome’. First, many of Ihe afo~eme~t~o~e~ floral characteristics can also be applied to flowers adapted to visitation by species other than non-flying mammals. For example, many traits (Box 2) are also suggestive of bat pollination. Second, such generalizations are often not upheld. In Australia, there are some 16 species of Banksiu and 18 species of ~~c~~y~~~s known to be visited regularly by nocturnal non-flying mammals. All of the eucalypts but only half of the banksias have a dull flower colour (cream, green, brown). Mo!:t species are also visited regularly by diurnal birds and inscc::;. For the few species that have been examined, timing of nectar production and s do not conform to the pattern predicted for a noctm rn~~a~~~ol~~~at~o~syndrome. Furthermore, some marsupials have also been documented as visiting flrwers that show a typical b~~~~-l~~~l~~~~ation syndrome (i.e. red colour and unscented nectar; Fig. I). Third, the n~)n~f~yi~gmammals that visit Blowers are extremely variable in behaviour and rno~~~~ofo~y,which may preclude selection for specific traits. Such mammals may be ~oct~~~al (all marsupials and roderuts) or diurnal (some primates), and range in size from the d~m~n~~tive(c. log) pygmy posstims (CercarfeetusL3’) of Australia to the largest (c. 15 kg) monkeys (BrachytelesZ1) from the neotropics. In areas with few nectar-feeding bats, it a some plants rely exclusively on non-flying mam lil~ation’:‘.?“,?!‘:“’ and that selection for specific has been exerted by these mammals. However, much more study is requirecl to understand how frequeat or widespread this situation is. oreover, it has been argued correctly that evolution in such systems has c perated unilaterallyL?N’z!l because these mammals also exploit other food types. Should we expect to see greater selection of traits where the relationship is ~~~l~q~~vocal~~ co evolution such as for those plants pollinated by the honey possum (Tilrsiples
-_.___
Many aljthors have argued that piants show
traitsthat
have coevo~veo ww ,100
predOmitlate ‘e.g. SouthAtma. SOtlthvvesi !&‘uslrrii Aubtral!d). cr,pi~c and gee florous floral traits Inlay bc selected for xt these conk !iltle advantage uhere arboreai species predominate (e.g. Rlodd.g~5~,ar, eastern Austra!;ai. An even stronger contrast is between nocturnal non-flying mammals that may select for dull flowers and pungent nectar, and diurmal mammals that may select for bright flov;srs and odourless nectaPz4. Rut whrch traits will he selected when both diurnal ano nncturnal species are present’“?
Dull flower colour Nocturnal anthesrs and nectar production Exserted stvle and stamens Pungent nectar Robust and/or compound flower structure Abundarlt nectar and ‘or pollen pmc!ui‘l~~~i Specific trai%s Dwnaf monkeys Brightly coloured flowers Non~pungent nectar Simultaneous flower opening Nocturn;~l leffestnal mamm~l.3 Nectar channelled to ground TI;;:t’r lrlflnlc!,r.i;lc,“, Geoflorous mflorescences Nocturnal arboreal mammcfs Non-crypW and non-geoflorous
rnflorescences
e foraging behaviour of pollinators will determine patterns of pollen flow in plant r,opmlations. it is imperative that we know more about the bre&ing amidmating systems ol plants visited by non-flying manrmma!s.Sonir assessment may also be needed of interspecific visits h~~auac in some areas the flowering times of plank may overlap. Without this type of information, it is ditficult to assess I~w importance of these mammals relative to otbtlr pollinators such as birds and ir.sects.
that project well out of the bounrlary layer - have not been well studied. This is ~~~~~~fy owing to two main factors: (1) the dilficulties of r~~eas~rf~~ wind in the field and separating its effects from the ~~1~~~~~~~~~ vadables of temperature and ~~~~~~ty: and (2) the expense involved in carrying out
chronic winds should be considered separately from the effects of rare wind events as hurricanes or stor SW events alter forest
e major storm events aP Forest, herIo 1938 storm in Harvard the 8991 ex~e~i~~e~t~f n Harvard Fnrent~ -
wind tunnel experiin the ~a~~~at~~y’,~ Nevertheless. much progress has been have ~e~~~~st~ate~ that stornns made recently in this field by a damage and kill climax and piorange of ~~ter~~s~i~~~~ary studies neer trees. Recovery after sue (many of which were reported a$ a storm involves resproutiug of the remit wdewrw ‘1: mucla is bkag dmaged trees. ~~~~~~l~~~~~y Bhe 4% -_ learned about the ~a~~str~~~~~c ma_x species. and massive growth A.R. Ennos is at the School of Biolog1ca6 Sc~enees, ellects of storms, and also about of seedings of pioneer species. Manchester University, 3.614 Stopford Building. the ~~c~irna~~ry and evolutionary Thus, the overaH effect of star Oxford Road. Manchester. UK Ml3 9PP. adaptations of individual trees to is, to some extent, to reverse the ~~~~-te~r~ esposure to windy conprocess of succession. ditions. This progress should help us to answer broader qe~tions on how the IQng-tern windregkne can affect the ecology and The chronic wind regime of a particular site probably diversity of forests. b.2~ 2 rztd:er iavoclr effrwf. nn --o[ogy. Though it &es _-_=-...A.._. V.. &v.T+ __ ._.,I ._L co;ltrolled
Wnts
ofthe species
under consideration are small, nocttlrnal and cryptic, necessitating the development of new techniques7J (Table 1, Many
Fig.
1). Other
species
rkr~ lal-ger.
flowers
non-destructively
com-
(Table 2). It is likely that there are still more species involved, particularly among ~0ct~rna~ mammals from places such as the neotropics and Asia, which have been relatively poorly studie Many plant species are involved in these interactions. VisitatiOi1 t0 flowers Of m0re than 85 species from 43 genera and 19 families has so far been documented (Table 3). The interaction appears to be particul lent in Australia, where visit a range of shrubs and trees from at least 59 species. Particular preference is shown for members
S.M. Carthew is at the Dept of Envlronmentai Science and Management. University of Adelaide, Roseworthy Campus, Roseworthy. South Australia, 5371 Australia; R.L. Goldmgay is at the School of Resource Science and Management, Southern Cross Univrrslty. PO Box 157 L~siiiorr. NSW 2480 bs;4ia”
ties are visited) and Myrfaceae (notably ~~c~ly~~~.~ of which at least 18 species are many other areas, a species is serviced b r example, in the neogenus ~ua~Q~i~~~ is visited by 12 species of
but are
found in more-remote areas that have not been well studied There have been a numbea until now’l. Recent studies in this of attempts to synthesize inforfield have focaisctl ~~~~~~~~~r~ly on 111Isuring the c~ffWti\~.Wt’ss rMion about the irlteraction between some groups of nonof these animals as pollinators. an three main types of data ale and the fiowers they visitr-4,1!‘. have been sought (Table 1). First, animals must be observed to visit flowers Second, rhey mu srantial loads of n and transport them to the flowers of a lack of c0rn~e~~~ion wi conspecific plants. nid, evidence is required to show that Australia, at least, ail m Ily pollinate flowers. and that such ~o~~~~ati0~~s
ted that a variety of mammals visited flowers across three continents; namely Australia, Africa ai”-!?. More recent stodiesl:i-lli have exer of species and have shown that it is even more comlinon and widespread than was first thought. There are now ~~e~~-~~c~I~entec~cases of ~~~~-f~yi~i~mammai ~o~~~~~at~0~~ ~~v[~~v~~~~ at Ieast 5y t~~~~~~~~ among 19 families and six ~?es~-~eprese~te~~groups are the ma *e 12 species, and the primate a. of which there are ni iie flower visitation by studied less often than for marsupials (I.5 versus 24 studies, not ~~c~ud~~ganecdotal accaunrs). there aDnear tn_ 170 m-r+ __.A.“.L species uf primates involved in pofl~nat~o~than any other ,OroW: 28 species of primates have been observed visiting
e 2). and at least some of visited by birds?. Other r indicates that ~~ecta~-~eedi~gbats may be Pp_esent with nonflying rnarnrna~s~:~~~4.~~~. TFhere have also been conflicting ideas about the imp0rtnnce of the interaction. For example, it is sometimes thought of as irncidental, with animals only visiliing flowers irrqplarlyl;. A~te~~~t~ve~y~plants may be visited by am array of gPoslinators”“,“,“, several of whi may be equally effective in p~~l~~at~~g~.For some plants mds may well act as the sole p particularly likeelyfor some of the plmts visited by lermrs in ~adagas~a~~~~,~4.~~ may be that these mamnaiian y~dlinators have shared a long utionary with the piants that ihcy visat, and that relation tes back to the Cretaceous3v4J4. However, this does not necessarily mean that the rehtionsbip is co-evolved.
Observations of flower visiting for nectar or pollen do not confirm that an animal is an effective pollinator. Data are required to demonstrate po?len transfer by mammaLs (Table 1). There are several ways this information can be obtained. Pollen can often be seen on the fur of foraging animals, since they typically get pollen all over their bead and bodyiJl,?‘l. Analysis of faecal samples further indicates that animals often ingest pollen during ctar feeding’“. This may incidental, or it may refl active feeding on polien6J4 or even regular grooming following nectar feeding”. Alternatively, pollen loads can be measured on captured animal r immediately after e or nder during foraging ntrolled conditions (Box 1). ates of pollen removal from
tWniber of studies Type of evidence
Il1ett,oc
Regular flower wsltatton
Direct obsen?at!ori Direct obscr;at;or,
Non-destructive Importance
Successful
feeding
of nectar and/or
pollen In diet
removal of pollen from flowers
Transportabon
of pollen 0’1 fur
P:e 1990
Post 1990
ir;ld
:3
~pt,~,i:
Trapping near flowers Remote cameras TracC+a 0
1 2 0 1
11 1 3 1 1
Direct observation Direct observation
- wld - captive
5 1
8 1
TImed obsenatlons Faecal analysis I>:etary requlrelments
wild
5
5
i
2
1
0
Pollen removal experiments
1
3
Dtrect observation Direct observatron
3 0 8
7 3 2
wild captlbe
Pollen loads Successful contact of sttgmas
Direct observabon
-wild
2
2
Movement between plants (showing ablkty to cross polilrlateI
Direct observabon Trackings’
-wild
6 1
6
Rdellty to a species
Direct observation I rddmg
1
0
Successful
pollmahon
Pollen germination
Successful
reproduction
Selective
3Tracktng includes the use of radiotracking,
nd compared with rates for OdS more acti~e~~.~. These tee WS t non-flying mammals pick up and carry large amounts of pollen, and are at least as good as other pollinators such as tive ~ol~~~ato~sthey must not ody must also deposit it ween conspecihic plants knowledge of the foraging behaviour of potentia ortant, as it will determine patterns of pollen flow are
spool-and-line
w~lrJ
1
0
1
experiments
0
2
seed set expenments
1
2
trackmg and fluorescen!
powder tracking
single tree for some time and empty systematically all flowers of nectar. However, species that a are most likely to efft *+self pollination. ecies occur in troops or family groups, and these may make regular inter-plant movements, dte~
tating cross-~oll~nat~o~l.
wav in which non f!ykg msmm~k fxage within and between
e of inter etween plants, and di
tances apart. For those smaller, less-mobile nectarivorous mammals, it may be advantageous to remain in a
g. 1. A waratah inflorescence (Telopea speciosissima) being visited by an eastern pygmy possum (Cercartetus nanus). The photograph was taken in the field usmg automated photography. The next photograph in the sequence showed ihe animal with its head buried in the back inflorescence.
l-able 2. .~ .~~ ~~ No. species
Otdt‘r
Family
hla:supidiik
Petauridae [Aust “1 iiasyt~tldae @St.; Eurramyldae (Ausr i
‘I i
Tarslpldidae Didelphldae 9,
1 2 3
5 :
&-ro~.‘,+m 1*a*c‘t . . L.L,-.“.’ (Aust.] (CA) (SAI
1 4. 1” 1 2
Rodentia
Mundae
(Aus1.i tSAfr.1 Gliric’ae (CAfr.1 Cricetldae $.?.I
Primates
CfArcopithecldae (CAfr l.orlsldae (CAfr.1 Galagidae [CAfr.) Ikmur~dar (Mad I C,ilIl:llrllltl,~c’ ,i.#\i II ISA! Cr~irlx! (CA1 ” is.4
II
1
+ 1 1 6, .3’ I” 5” 3 1, 4
Scandt~ntl~~
1tl&II!liCiU iG”fll
1
Carnlvold
V~verriilx(Ci\bI
Plocva~l’:lcle (C4’!
1 2
Macrosceklea
Macroscelldldae
1
Aust.. Austrak:
CA, Central America: SA. South America; SAfr.. South Alrica: CAfr.. GSI. Greater Sunda islands diurnal species. all other species are nocturnal.
CentralAfrica: Mad.. Madagascar: “Indicates
(Skft.)
rroteaccae Myriaceae Rul acoalr S~iplnd.W<.lc h
showing traulininti behaviour !s. In some instances, araimals may n&e qbite long distances between visits, avoiding near neighbours, for presumably more rewarding plants. Species that visit a few flowers on a plant in quick succession and carry pollen over long distances are likely to effect crosspollination and promote more long-distance gene flow. Flower visitors may also vary their behaviour during a flowering season. For example, in one study on the gliding mars3pial (Pelu~r~ austr~lis), Goldingay?” found that when [lowers were scarce, animals were forced to make longdistence movements (often more than 50 m) between trees, but tended to stay in a single tree for long periods. Conversely, when flowers were abundant, animals spent ler,s time in individual trees but moved between ~eig~bo~~;~g trees. This indicates that pollen flow may vary throu# a season, and thus have imporlant imphcations for gene exchange, particularlly in those @ants that are self-compatible.
nammals Bead to the production of seed? IT1 sonW instanr-s it Cilll be ~kssuY71cc~ that non-Ilying n~ammais are ~o~~~~at~ng effectively because of the morphological fit between pollinator and flower (e.g. POi SOI1K” Bemursz:~). However, it is difficult to conduct experiments that show conclusively that non-flying mammals are capable of effective pollination. or that they are ‘better’ pollinators than other visitors. This requires a comparison of the proportional co~tr~bnt~o~ ~f~o~~-~~y~~g mammals to pollination with that for all other flower visitors. Selective exclusion experiments can be conducted, whereby non-flying maminals are rxcludetl from visiting flowers that all other pollinators can access. To date, the method has been used on only a few species of the Proteaceae. dunksi~ spr’nuloso ar:d B. j~te~~~~~li~ hnm Australia”-7 and Proreu a~n~~~x~call~isand P ~?ur~~~~l~~~~ from South Africaz!‘. For R. spinuloscr.experiments revealed that marsupials are at least equally as effective as birds at jri~llill;itiug firw~~rs. ;tnd at litales Iuay be better than their avian coePnterparts’i.T.Wiens et al.‘!‘showed that fruit set on ii r&t 4 Pr’1.01~ was reduced by up to 5fPX, on ina’lorescences whcrc manmnai visitation was excluded. The reason that so frw attempts have been: made to assess the effectiveness of il~iU~Il)~illi~llp~SlilI~~tOlSis tllat tllc PlalIP SpCckS invOlvct8 often exhibit low levels of natural fruit set or have flowers that are inaccessible or difficult to cage (e.g. mass-flowering trees).
bhXOSacede Cappandaceae Combretacede
Bombacaceae Euphorblaceae Guttlferae Musaceae Acanthaceae Cilrvsobalanaceae
(timing of flower opening. pollen ~~~~se~~tati~)~ and nectar secretion) hail traits as adaptations to ~o~l~~~at~~~~~ by ~~~)~~~f~y~~~g mammals (Box 2). For example. flowers are often large and robust IS.23 (to cope with large and sometimes vigorous feeders), or presented as multi-flowered inflorescenc&.l1.~1-2:{. iBecame many non-flying mammals are ljocturnal and iPilW acute olfactory senses, flowers are often drab in colku~tii:& :,‘L .l.mib~~ Of poiien glalils sdliipied frOrl1 the lied& of fiord1 vlsltors has been used Lo d~sebs bl!Js dn\l no11QLn”‘~‘~~? “I, but exude a punflying mammal5 for their llotent~al as pollmators~~. Such studies report birds with pollen loads of several thousand gralns and gent odo~r~~~~l. To provide a mammals ~th Pollen loads of a few hundred grams. However. these samgles are scarcely comparable because mammals were sampled aiIer remaining m traps overnight, while bards were sampled soon after capture In mist net+. Morepredictable and worthwhile Precise assessment Of pollen loads has involved sampling pollen from mammals trapped at l-3 ii Intervals and also after resource for mammals, piants hand capture’. .“. ComParlSon with mammals sampled after about Xh in haps showed that pollen loads decreased draoften flower profusely and mdtlca@ Ihe lorlrSer mammalsstayedIntraps. indlcatmg removal during groomingz’. Sampling oftwo marsupiais ~Ankci,:produce copious amounts flus stuart~~ and Waurus brevicepslwithln 1 h of capture has revealed total pollen loads of 3000-15 000 pollen grains of sugar-rich ~e~f~~l4.1W.2~3~ Per bead’. This value suggests conslderable potential to effect pollmatton. They should comparatively
also produce large amounts
of poller~~‘~,because
mam are often larger than other pollinators (which may red precision in pollen delivery and transfer] and- some s ies include @ilen in their dieP. Despite these generatizations, there can be no allencompassing ‘non-flying mammal pollination syndrome’. First, many of Ihe afo~eme~t~o~e~ floral characteristics can also be applied to flowers adapted to visitation by species other than non-flying mammals. For example, many traits (Box 2) are also suggestive of bat pollination. Second, such generalizations are often not upheld. In Australia, there are some 16 species of Banksiu and 18 species of ~~c~~y~~~s known to be visited regularly by nocturnal non-flying mammals. All of the eucalypts but only half of the banksias have a dull flower colour (cream, green, brown). Mo!:t species are also visited regularly by diurnal birds and inscc::;. For the few species that have been examined, timing of nectar production and s do not conform to the pattern predicted for a noctm rn~~a~~~ol~~~at~o~syndrome. Furthermore, some marsupials have also been documented as visiting flrwers that show a typical b~~~~-l~~~l~~~~ation syndrome (i.e. red colour and unscented nectar; Fig. I). Third, the n~)n~f~yi~gmammals that visit Blowers are extremely variable in behaviour and rno~~~~ofo~y,which may preclude selection for specific traits. Such mammals may be ~oct~~~al (all marsupials and roderuts) or diurnal (some primates), and range in size from the d~m~n~~tive(c. log) pygmy posstims (CercarfeetusL3’) of Australia to the largest (c. 15 kg) monkeys (BrachytelesZ1) from the neotropics. In areas with few nectar-feeding bats, it a some plants rely exclusively on non-flying mam lil~ation’:‘.?“,?!‘:“’ and that selection for specific has been exerted by these mammals. However, much more study is requirecl to understand how frequeat or widespread this situation is. oreover, it has been argued correctly that evolution in such systems has c perated unilaterallyL?N’z!l because these mammals also exploit other food types. Should we expect to see greater selection of traits where the relationship is ~~~l~q~~vocal~~ co evolution such as for those plants pollinated by the honey possum (Tilrsiples
-_.___
Many aljthors have argued that piants show
traitsthat
have coevo~veo ww ,100
predOmitlate ‘e.g. SouthAtma. SOtlthvvesi !&‘uslrrii Aubtral!d). cr,pi~c and gee florous floral traits Inlay bc selected for xt these conk !iltle advantage uhere arboreai species predominate (e.g. Rlodd.g~5~,ar, eastern Austra!;ai. An even stronger contrast is between nocturnal non-flying mammals that may select for dull flowers and pungent nectar, and diurmal mammals that may select for bright flov;srs and odourless nectaPz4. Rut whrch traits will he selected when both diurnal ano nncturnal species are present’“?
Dull flower colour Nocturnal anthesrs and nectar production Exserted stvle and stamens Pungent nectar Robust and/or compound flower structure Abundarlt nectar and ‘or pollen pmc!ui‘l~~~i Specific trai%s Dwnaf monkeys Brightly coloured flowers Non~pungent nectar Simultaneous flower opening Nocturn;~l leffestnal mamm~l.3 Nectar channelled to ground TI;;:t’r lrlflnlc!,r.i;lc,“, Geoflorous mflorescences Nocturnal arboreal mammcfs Non-crypW and non-geoflorous
rnflorescences
e foraging behaviour of pollinators will determine patterns of pollen flow in plant r,opmlations. it is imperative that we know more about the bre&ing amidmating systems ol plants visited by non-flying manrmma!s.Sonir assessment may also be needed of interspecific visits h~~auac in some areas the flowering times of plank may overlap. Without this type of information, it is ditficult to assess I~w importance of these mammals relative to otbtlr pollinators such as birds and ir.sects.
that project well out of the bounrlary layer - have not been well studied. This is ~~~~~~fy owing to two main factors: (1) the dilficulties of r~~eas~rf~~ wind in the field and separating its effects from the ~~1~~~~~~~~~ vadables of temperature and ~~~~~~ty: and (2) the expense involved in carrying out
chronic winds should be considered separately from the effects of rare wind events as hurricanes or stor SW events alter forest
e major storm events aP Forest, herIo 1938 storm in Harvard the 8991 ex~e~i~~e~t~f n Harvard Fnrent~ -
wind tunnel experiin the ~a~~~at~~y’,~ Nevertheless. much progress has been have ~e~~~~st~ate~ that stornns made recently in this field by a damage and kill climax and piorange of ~~ter~~s~i~~~~ary studies neer trees. Recovery after sue (many of which were reported a$ a storm involves resproutiug of the remit wdewrw ‘1: mucla is bkag dmaged trees. ~~~~~~l~~~~~y Bhe 4% -_ learned about the ~a~~str~~~~~c ma_x species. and massive growth A.R. Ennos is at the School of Biolog1ca6 Sc~enees, ellects of storms, and also about of seedings of pioneer species. Manchester University, 3.614 Stopford Building. the ~~c~irna~~ry and evolutionary Thus, the overaH effect of star Oxford Road. Manchester. UK Ml3 9PP. adaptations of individual trees to is, to some extent, to reverse the ~~~~-te~r~ esposure to windy conprocess of succession. ditions. This progress should help us to answer broader qe~tions on how the IQng-tern windregkne can affect the ecology and The chronic wind regime of a particular site probably diversity of forests. b.2~ 2 rztd:er iavoclr effrwf. nn --o[ogy. Though it &es _-_=-...A.._. V.. &v.T+ __ ._.,I ._L co;ltrolled
Wnts