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Acta Oecologica 65-66 (2015) 17e23

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Acta Oecologica

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Original article

Humid microclimates within the plumage of mallard ducks(Anas platyrhynchos) can potentially facilitate long distancedispersal of propagules

Neil E. Coughlan*, Tom C. Kelly, John Davenport, Marcel A.K. JansenSchool of Biological, Earth and Environmental Sciences, University College Cork, Cork, Ireland

a r t i c l e i n f o

Article history:Received 11 November 2014Received in revised form28 March 2015Accepted 31 March 2015Available online

Keywords:EpizoochoryDispersalPlumageHumidityMallard duckLemna

* Corresponding author.E-mail address: neil.coughlan.zoology@gmail.com

http://dx.doi.org/10.1016/j.actao.2015.03.0031146-609X/© 2015 Elsevier Masson SAS. All rights res

a b s t r a c t

Birds as carriers of propagules are major agents in the dispersal of plants, animals, fungi and microbes.However, there is a lack of empirical data in relation to bird-mediated, epizoochorous dispersal. Themicroclimate found within the plumage likely plays a pivotal role in survival during flight conditions. Toinvestigate the potential of epizoochory, we have analysed the microclimatic conditions within theplumage of mallard ducks (Anas platyrhynchos). Under similar ambient conditions of humidity andtemperature, a sample of mallards showed a consistent microclimatic regime with variation across thebody surface. The highest (mean) temperature and specific humidity occurred between feathers of thepostpatagium. The lowest humidity was found between feathers of the centre back and the lowesttemperature in the crissum. Observed differences in plumage depth and density, and distance from theskin, are all likely to be determining factors of microclimate condition. Specific humidity found withinthe plumage was on average 1.8e3.5 times greater than ambient specific humidity. Thus, the plumagecan supply a microclimate buffered from that of the exterior environment. Extrapolating survival data forLemna minor desiccation at various temperature and humidity levels to the measured plumage micro-climatic conditions of living birds, survival for up to 6 h can be anticipated, especially in crissum, cruraland breast plumage. The results are discussed in the context of potential long distance epizoochorousdispersal by A. platyrhynchos and similar species.

© 2015 Elsevier Masson SAS. All rights reserved.

1. Introduction

Birds as carriers of propagules are major agents in the longdistance dispersal (LDD) of plants, animals, fungi and microbes(Green and Elmberg, 2014). Darwin (1859) suggested that waterbirds dispersed freshwater plants; he also demonstrated experi-mentally that ducks were potential dispersers of freshwater snails.As part of their migratory movements, birds often travel long dis-tances in relatively short periods of time (Clausen et al., 2002;Brochet et al., 2010). Teal (Anas crecca), for example, have beenknown to cover an average of 100 km per day and potentially up to1000 km within a few days, while pintail (Anas acuta) have trav-elled 1,600 km within 24 h (Clausen et al., 2002). Even if only aminority of individuals participate in the transporting of propa-gules, the impact may be substantial considering the thousands of

(N.E. Coughlan).

erved.

birds travelling long distances annually, and the even largernumbers travelling shorter distances (Charalambidou et al., 2003;Brochet et al., 2010).

The successful dispersal of an organismwill be governed by theability of its propagule to survive the transportation process(Figuerola et al., 2010). Plumage is thought to play a key role inepizoochorous dispersal. Evidence suggests that the moisturecontent (humidity) found within-plumage can influence the suc-cess of an epizoochorous event, with higher humidities reducingthe rate of desiccation and therefore maintaining propaguleviability for longer periods (Coughlan et al., 2015). Currently,however, there is a lack of empirical data in relation to bird-mediated, epizoochorous dispersal (Costa et al., 2014). Additionalinformation is required in order to evaluate the likelihood of suc-cessful transportation of propagules by birds, and their survival inthe associatedmicroclimatic conditions. It is especially necessary togain an understanding of the temperature and moisture i.e. hu-midity regimes that exist within the plumage of birds. Dispersalkernel modellers need to know the conditions experienced during

N.E. Coughlan et al. / Acta Oecologica 65-66 (2015) 17e2318

transport and the survival of propagules under those conditions.Species-specific dispersal distances (e.g. daphnia resting eggs,snails and aquatic plants) may then be predicted.

Plumage is the most complex integumentary structure of ver-tebrates and is characteristic of birds (Stettenheim, 2000; Broggiet al., 2011). Plumage is comprised of unique, complex, non-livingoutgrowths known as feathers (Stettenheim, 2000; Tickell, 2003)which, in addition to enabling lift and propulsion for flight, alsoprovides for inter alia, thermal insulation, streamlining, water-proofing, social communication and camouflage (Stettenheim,2000; Tickell, 2003; Broggi et al., 2011). Downy feathers providethermal insulation by trapping air close to the skin (Stettenheim,2000). Larger contour feathers also provide insulation and can beadjusted to partially regulate body temperature (Stettenheim,2000). In effect a thermal buffer is created between the bird andits surroundings. Birds primarily lose heat to the ambient envi-ronment by non-radiative heat flow through conduction and con-vection (Walsberg, 1988) and an almost complete thermal gradientbetween skin temperature and environment can be attained withinthe plumage (Davenport et al., 2004). Feather abundance andstructure crucially determine the buffer's ability to minimise heatloss, set an upper limit to insulation capacity and, in part, regulateheat loads from solar radiation (Wolf and Walsberg, 2000; Broggiet al., 2011). The ability to create a thermal buffer can be essentialfor avian survival when environmental conditions are unfavourable(Brodin, 2007). Similarly, the loss of water vapour from the integ-ument of an organism to the ambient environment depends on thenature of the barrier to evaporation, the concentration of watervapour at the evaporating surface, and the humidity of the air(Webster et al., 1985). Body regions differ in their degree of insu-lation and therefore variations in microclimate over the entireanatomy of the body are to be expected (Webster et al., 1985).

Many organisms will exploit the plumage and its thermal bufferzone for dispersal, or as a permanent habitat. Birds are host tomanyparasites including a wide range of medically and veterinarilyimportant ectoparasites (Clayton and Moore, 1997; Atkinson et al.,2008). The composition of epifauna found within the plumage isgoverned by many variables, including inter alia, host behaviour,ecology, anti-parasite defences and parasite competition (Claytonand Walther, 2001). Ectoparasites living within or beneath theplumage will be directly exposed to plumage microclimatic con-ditions (Moyer et al., 2002). For instance, the distribution of lice(Phthiraptera) (Clayton, 1991; Clayton et al. 2008) and mites(Arachnida) (Bonser, 2001; Pence, 2008) between, and within,feathers will be influenced by microhabitat properties such as hu-midity and temperature (Mestre et al., 2011). In his seminal workYu. S. Balashov (1968) observed the behaviour and survival of ticksunder varied conditions of relative humidity and temperature. Hehypothesised that bird parasitizing species with long feeding pe-riods will have a greater potential for dispersal, and that migratorymovements of birds can account for the wide distribution of someArgas species and other bird parasites. Indeed, it is the opinion ofHoogstraal et al. (1961, 1963, 1964) that there is an influx of Africantick subspecies into Europe and northern Asia in the spring, and anefflux in autumn, facilitated by transmigrating birds (Balashov,1968).

In this study the microclimate within the plumage of mallardducks was examined. The mallard is the most abundant andwidespread dabbling duck species in the world, with a globalbreeding population estimated to be at least 18 million birds(Delany and Scott, 2006; S€oderquist et al., 2013). The species iscomprised of both sedentary and migratory populations, thoughbirds in both groups will frequently intermingle (Delany et al.,2006). As an economically important quarry species, wild stocksare heavily augmented with farmed birds (Guillemain et al., 2010;

S€oderquist et al., 2013). Given their ecology, water birds in partic-ular are considered leading contributors to bird mediated dispersal(Costa et al., 2014; Green and Elmberg, 2014; Coughlan et al., 2015).

We hypothesised that a microclimate exists within the plumage,where temperature and humidity remain reasonably constant,which can facilitate plant propagule survival. In this study surfacetemperature and humidity within the plumage of mallard (Anasplatyrhynchos) were measured. To link the identified microclimaticregimes with propagule survival, we examined the survival andviability of a common aquatic plant Lemna minor under similarconditions to those observed within the mallard plumage. The re-sults reveal the relative suitability of different areas within theplumage for propagule survival.

2. Methods

2.1. Examination of temperature and humidity

Five game-farm reared mallards were acquired and kept in alarge, out-door, free-range enclosure (15 m � 3 m � 3 m), whichincluded a housing unit for shelter and an artificial pond. Themallards were investigated in the spring of 2013 on three separateoccasions; in each experiment three birds were sampled. All birdswere sampled at least once, no bird was examined twice on a singleoccasion. Subsequently, five more birds were added to the enclo-sure. All ten individual mallards were investigated in the spring of2014, each bird on a separate occasion. All birds had been out ofwater for at least 120 min before monitoring of the microclimatewithin the plumage commenced. Birds were held in the hands of anoperative, while a second operative examined the microclimaticconditions. Restraint of the birds in this manner did not interferewith the examined anatomical areas, nor cause stress as the birdswere used to handling.

A dual hygrometer/thermometer (Fisher Scientific, 11-661-18,Waltham, MA, USA) was used for the measurement of plumagetemperature (�C) and relative humidity (%RH). The portion of theinstrument probe which needed to be inserted within the plumagewas 20 mm long and 13 mm wide. The end of the probe, whichprotects the sensors, is plastic with 8 slots, each 3 mmwide. Areassuch as the breast and back were sampled with the probe held atacute angles to the plumage to allow for full immersion of the probewithin it. Readings were taken from as close to the skin as possible.The probe remained in place until microclimatic conditions wereobserved to recover and stabilise. This took several minutes. Thebirds were examined in the field, ambient temperature and relativehumidity were recorded in both 2013 (11.2 ± 1.1 �C; 69.4 ± 4.8% RH)and 2014 (10.2 ± 0.7 �C; 70.6 ± 1.3% RH) (mean ± SE) at the time ofthe experiments.

Multiple areas were examined on all individuals in order tocompile an overall map of the temperature and humidity rangesfound on the birds. The anatomical areas (see Fig. 1) investigatedincluded the posterior neck (dorsal), the centre breast, the centreback, either side of the tail within the undertail coverts (crissum),both wings under the postpatagium, and within the crural plumageof the inner legs. Readings were taken at the wing with the probepositioned under the postpatagium and with wings naturally fol-ded closed against the body. Postpatagium and crural plumageswere examined in 2014 only. The external atmospheric tempera-ture and relative humidity were also measured both before andafter the experimental protocol had been completed.

2.2. Examination of plumage depth

To quantify differences in plumage structure across the anatomyof the mallard, depth of plumage was examined using vernier

Fig. 1. Relative humidity (% RH), mean þ SE, observed within the plumage of mallardduck. Neck, back and breast, n ¼ 19. Wing and crural, n ¼ 20. Crissum, n ¼ 38.

N.E. Coughlan et al. / Acta Oecologica 65-66 (2015) 17e23 19

callipers. The stem of the callipers was gently inserted into theplumage and positioned as close to bare skin as possible. The stemwas held gently and as perpendicular as possible against the skin.The base of the vernier callipers was then brought into contact withthe outermost plumage and ameasurement was recorded. This wasdone for each of the examined areas of plumage on five randomlyselected individuals. No bird was sampled twice. In the case of theinner crural, the stem was inserted into the pit of the leg. Plumagefeather type composition was also judged by the gentle back-combing of plumage by hand.

2.3. Lemnaceae cultures

Axenic cultures of L. minor were maintained on half-strengthHutner's growth medium in 100-ml magenta vessels in acontrolled environment growth room (Lahive et al. 2011). Thestandard conditions for plant culturing were 16-h light: 8-h dark-ness at a light intensity of 50 mmol m�2 s�1 (cool white fluorescentlamps) and a temperature of 22 ± 2 �C. L. minor had been collectedlocally (Blarney, Co. Cork, Ireland).

2.4. Desiccation and survival experiments under ex situ conditions

Following the method outlined in Coughlan et al. (2015), L. mi-nor colonies were removed from the magenta vessels and excessmedia gently was removed using filter paper. Damp colonies werethen spread out: (a) on glass plates, representing severe droughtstress; (b) in plastic containers between two layers of two to fourfeathers of mallard plumage (obtained from the breast, back,crissum and neck of deadmallard provided by game-hunters) or (c)in plastic containers between two layers of two to four feathers ofmallard plumage resting on a double layer of damp to saturatedfilter paper. Samples were returned to fresh growth medium atregular 1-h intervals for up to 25 h to quantify drought survival andviability under stagnant air conditions. At each time point, sixreplicates, comprised of four colonies of two fronds, were taken.Control samples were directly transferred between magenta ves-sels, without exposure to drought. Resumption of growth afterdrought stress was measured as an increase in the number of col-onies, fronds and biomass after 7 days under standard growthconditions. The relative humidity and temperature were recordedat regular intervals within the containers fromwithin the plumage,using a dual hygrometer/thermometer (Fisher Scientific, 11-661-18,

Waltham, MA, USA). If humidity began to decrease, very smallamounts of deionised water were added to a far corner of thecontainer and its lid was closed until humidity had recovered. Ifhumidity began to increase, the lid of the container was removed.The experiments were conducted under ambient room tempera-ture (21.7 �C ± 0.74SD, range ¼ 20.6 �Ce23.1 �C).

2.5. Specific humidity calculations

Relative humidity (RH%) is a percentage of the maximumpossible carrying capacity (absolute humidity) of the air at a giventemperature. The maximum absolute humidity will vary atdifferent temperatures. When calculated as specific humidity ameasurement of water content in grams per kilogram of air isproduced. Specific humidity (1) was calculated under standard at-mospheric pressure, 1013.25 hPa, using the observed relative hu-midity and temperature.

Specific humidity

Q ¼ 1000 Pv=ð1:6078 Pb� 0:6078 PvÞhg kg�1

i(1)

where:

Pv¼ Partial pressure of water vapour [Pa] See Eq. (2)Pb¼ Total or barametric pressure¼ 101,325 Pa

Partial pressure of water vapour

Pv ¼ fPsat (2)

where:

Pv¼ Partial pressure of water vapour [hPa]f¼ Relative humidity (%)Psat¼ Saturation vapour pressure [hPa] See Eq. (3)

Saturation vapour pressure

Psat ¼ 6:1078� 107:5T

Tþ237:3 (3)

where:

Psat¼ Saturation vapour pressure [hPa]T¼ temperature [�C]

2.6. Statistical analysis

Data were analysed using one-way ANOVAs with the post-hocTukey HSD in SPSS (version 20; SPSS Inc, Chicago, IL, USA). MultipleANOVAs with different dependent factors were performed. Tem-perature and specific humidity were both examined separately foreach body location, with data from each individual area taken as adependent factor and year of experiment as the random factor.Subsequently, plumage temperature and specific humidity (exam-ined separately) were tested across the body surface, withmeasured data from all combined body locations as the dependentfactor for both. Plumage depth was likewise calculated with bodylocations as the random factor. L. minor survival and viability wereexamined with the random factor of time and the dependent factorof the numbers of colonies, fronds and the biomass. All factors wereexamined separately for each experimental humidity. Post-hocanalysis was conducted for all ANOVAs which compared more thantwo groups.

N.E. Coughlan et al. / Acta Oecologica 65-66 (2015) 17e2320

3. Results

Ambient air conditions of temperature and the calculated spe-cific humidity at the time of the experiments in 2013 (11.2 ± 1.1 �C;5.6 ± 0.3 g kg�1) and 2014 (10.2 ± 0.7 �C; 5.5 ± 0.3 g kg�1)(mean ± SE), were not statistically different; temperature(F1,17 ¼ 0.697, P > 0.05), specific humidity (F1,17 ¼ 0.15, P > 0.05).Likewise the temperature and specific humidity profiles on themallards were found to be similar at each of the body locationssampled in 2013 and 2014 and so the data from these experimentswere pooled (Table 1).

Temperature and specific humidity were higher in both thepostpatagium and crural plumage (temperature F5,129 ¼ 33.366,P < 0.01; humidity F5,129 ¼ 55.741, P < 0.01), compared with otherlocations on the birds (Fig. 2). The postpatagium and crural plum-ages were similar in relation to specific humidity, but the temper-ature at the former location was significantly higher. In the case oftemperature, the neck and crissum were also found to be margin-ally different (F5,129 ¼ 33.366, P ¼ 0.044) from each other. The neck,back, crissum and breast plumage of the mallards were similar inrelation to specific humidity. Temperature was similar at the neck,back and breast of the birds.

The postpatagium displayed both the highest temperature(33 ± 0.8 �C) and specific humidity (19 ± 0.93 g kg�1), the centreback the lowest humidity (10 ± 0.72 g kg�1) and the crissum thelowest temperature (21 ± 0.66 �C) (mean ± SE). All other areasshowed very similar values of specific humidity and temperature(Fig. 2).

Specific humidity found within the plumage was on average1.8e3.5 times greater than ambient humidity. Average specifichumidity of each body location was examined against the averageexterior specific humidity. Mean relative humidity values (±SE)were highest at the inner crural and crissum (72.1 ± 3.4 and72.8 ± 2.1%) and lowest at the centre back (58.4 ± 2.9%) (Fig. 1).

While examining the birds it was noted that %RH oftendecreased with increasing temperature, particularly at the post-patagium and inner crural. Specific humidity was found to increasewith increasing temperature (Fig. 3).

Fig. 2. (A) Temperature (�C) and (B) specific humidity (g kg�1), mean þ SE, observedwithin the plumage of mallard duck. Posterior neck, centre back and breast, n ¼ 19;postpatagium and inner crural, n ¼ 20; crissum, n ¼ 38. (C) Plumage depth (mm),mean þ SE, observed in different areas the surface anatomy of mallard duck (n ¼ 5).Corresponding symbols indicate statistical similarity, otherwise each anatomicallocation is statistically different from all others. Dashed line represents ambienttemperature (A) and specific humidity (B).

3.1. Examination of plumage depth

Mallards displayed significantly different depths of plumageacross the different areas (F5,24 ¼ 66.64; P < 0.0001) (Fig. 2). Thepostpatagium and the back had the most shallow plumage, whilethe crural and the crissum had the deepest plumage. The crissumand posterior neck were marginally non-significantly different(Table 2). Each of the examined areas differed in their compositionof feather type's viz. downy (plumulaceous) and contour feathers(pennaceous). Some areas, for example the crural and crissum, hadgreater amounts of downy than contour feathers, while other areas,such as the back and neck, had more contour feathers (pers. obs.).

Table 1Temperature and specific humidity profiles on the mallard ducks were found to bestatistically similar at each of the body locations sampled in the spring of 2013 and2014.

Body location Temperature Specific humidity

Posterior neck (F1,17 ¼ 1.7, P > 0.05) (F1,17 ¼ 0.896, P > 0.05)Centre back (F1,17 ¼ 0.685, P > 0.05) (F1,17 ¼ 0.591, P > 0.05)Centre breast (F1,17 ¼ 1.558, P > 0.05) (F1,17 ¼ 0.47, P > 0.05)Postpatagium 2014 only 2014 onlyInner crural 2014 only 2014 onlyCrissum (F1,36 ¼ 3.492, P > 0.05) (F1,36 ¼ 1.7, P > 0.05)

3.2. Desiccation and survival under ex situ conditions

L. minor colonies were removed from the magenta vessels andspread out: (a) on glass plates; (b) in plastic containers betweentwo layers of two to four feathers of mallard plumage; and (c) inplastic containers between two layers of two to four feathers ofmallard plumage resting on a double layer of damp to saturatedfilter paper. Under these three experimental conditions the relativehumidity (RH) was 47.2 ± 1.4%, 66.9 ± 2.2% and 98.8 ± 0.3% (max99.9%), (mean ± SE) respectively. Mean temperature (±SE) was21.2 ± 0.1 �C, 21.6 ± 0.1 �C and 21.6 ± 0.2 �C respectively. Whencolonies were exposed to a low RH, L. minor viability decreasedsignificantly with increasing time outside the medium (Fig. 4). Thelonger L. minor was kept outside the medium, the lower thenumber of colonies (F4,25 ¼ 48.87; P < 0.01), fronds (F4,25 ¼ 62.19;

Fig. 3. Specific humidity (A) was observed to increase with increasing temperature(y ¼ 0.669x � 3.253), while relative humidity (B) was observed to decrease withincreasing temperature within the plumage of mallards. (y ¼ �0.633x þ 82.54).

Table 2Plumage depth of the mallard ducks was found to vary significantly with anatomicalposition on the body.

Body location Depth Significance

Centre back Most shallow (F5,24 ¼ 66.64; P < 0.0001)Postpatagium Most shallow (F5,24 ¼ 66.64; P < 0.0001)Inner crural Deepest (F5,24 ¼ 66.64; P < 0.05)Crissum Deepest (F5,24 ¼ 66.64; P < 0.001)

Fig. 4. Formation of new colonies (A), fronds (B) and biomass (C) by drought-stressedLemna minor (mean ± SE). Plants were drought stressed for up to 2 h at 47.2 ± 1.4%(A), 6 h at 66.9 ± 2.2% (-) and 25 h at 98.8 ± 0.3% (:) (mean ± SE). Mean tem-perature (±SE) was 21.2 ± 0.1 0.2 �C, 21.6 ± 0.1 �C and 21.6 ± 0.2 �C respectively. Af-terwards, four colonies of two fronds were returned to the medium and growthassessed after 7 days (n ¼ 6).

N.E. Coughlan et al. / Acta Oecologica 65-66 (2015) 17e23 21

P < 0.01) and biomass (F4,25 ¼ 196.71; P < 0.01) produced by frondsreturned to the medium. No viability was detected when L. minorhad been retained for more than 120 min out of the medium(Fig. 4). In contrast, when colonies were kept under a more mod-erate humidity, viability was retained for a considerably longerinterval. Even after 5 h outside the medium, viable fronds werenoted (Fig. 4). The number of colonies (F6,35 ¼ 20.69; P < 0.01),fronds (F6,35 ¼ 35.11; P < 0.01) and biomass (F6,35 ¼ 58.15; P < 0.01)produced following return to growth medium all displayed a verygradual decline with increasing time out of the medium. WhenL. minor was kept under high RH, an initial decline in colonynumber, frond number and biomass occurred after fronds had beenremoved from the medium for an interval of 1 h. Thereafter colonyand frond numbers and biomass were stable (Fig. 4).

4. Discussion

4.1. Mallard plumage displayed anatomical variations inmicroclimatic regime

In this study mallards showed a consistent microclimate (tem-perature and humidity) within their plumage when exposed toidentical ambient conditions. However, some anatomical variationwas observed. For example, the postpatagium had the highest(mean) temperature and specific humidity, while the centre-backhad the lowest humidity and the crissum the lowest temperature.Elevated temperatures corresponded to decreased relative hu-midity but increased specific humidity (Fig. 3).

Plumage depth does not on its own explain the anatomicalvariation in microclimate. The postpatagium and crural plumage

displayed a very similar microclimate, however these areas differedsubstantially in plumage depth (Fig. 2). Feather type, density anddepth differ anatomically, therefore variation in insulation is ex-pected (Webster et al., 1985; Porter et al., 2000). Certainly thecentre back, observed to have some of the shallowest and the leastdense plumage of the examined areas, showed the lowest specifichumidity of the different anatomical areas. Future studies shouldmore specifically examine variation in microclimatic conditionsdue to plumage type. Distance from skin is also likely a determiningfactor of microclimatic conditions within the plumage. The densityof feather elements is lowest near the skin and greatest at the

N.E. Coughlan et al. / Acta Oecologica 65-66 (2015) 17e2322

feathereair interface (Porter et al., 2000). Some areas, such as thecrissum, are covered by a deep and dense plumage. It is likely thatin such circumstances microclimatic measurements are those ofthe plumage rather than that at the level of the skin. Increased heattransfer from the birds' skin likely accounts for the higher surfacetemperature and specific humidity observed at the postpatagium.This is seen once againwithin the inner crural, where the probewasin direct contact with the tarsus. At these locations the probe wasboth in close contact with the skin and well sheltered by plumage.Thus a gradient across the plumagemicroclimate is presented here.The level of the skin is likely best represented here by the post-patagium and crural examinations. The middle inter plumage zonebeing represented by the other examined areas.

4.2. Plumage appears capable of buffering against low ambienthumidity

Moyer et al. (2002) found within-plumage RH to be highlycorrelated with ambient RH for captive pigeons, and concluded thatplumage does not act as an effective humidity buffer. A somewhatsimilar trend between ambient and plumage RH was also observedin our study of mallard ducks. However, in this case, specific hu-midity was found to be significantly higher within-plumage than inthe ambient environment. Specific humidity within the plumagewas on average 1.8e3.5 times greater than ambient specific hu-midity. Higher specific humidity corresponded with higher within-plumage temperatures. It appears that plumage can buffer thesurface microclimate of mallard ducks against low ambient hu-midity. There is likely a species-specific element that explains thisdifference; waterfowl plumage probably has greater insulatingproperties than that of pigeon, due to differences in plumagestructure corresponding with their respective ecologies (Dove andAgreda, 2007; Dove et al., 2007; Rijke and Jesser, 2011).

Quantitative studies on desiccation of biota were pioneered byEdney (1951), but were conducted under conditions of negligibleairflow rate. Therefore, Edney (1951) allowed shells of moistmicroclimate to persist around the test material. A study by Kensler(1967) revealed that air-flow dissipates the moist boundary layersbetween an organism and the true external environment, hencecausing greatly enhanced water loss at RH values <100%. Kensler(1967) also showed that size of the tested organism was impor-tant e small animals dried out much more quickly than largeranimals when exposed to moving air of reduced RH. This wasconfirmed by Davenport and Vahl (1983). However, bird plumageappears to be ideally suited to minimizing airflow over smallpropagules; its microporosity means that the air within theplumage is probably stagnant for most of the time, allowing moistshells to persist around damp propagule material.

4.3. The impact of desiccation stress depends upon the level ofhumidity exposure

In relation to dispersal, plumage provides a means of attach-ment and ensnarement for organisms and propagules (Raulingset al., 2011). Coughlan et al. (2015) demonstrated that L. minormanually placed between feathers on a live duck can be retained byfree-roaming birds for over 2 h. Any propagule that is entangledbetween feathers will be exposed to the microclimate of theplumage. In keeping with the findings of Coughlan et al. (2015) onthe survival of desiccation stressed Lemna minuta, desiccationstress was found to depend upon the level of humidity exposure. Ata low humidity (47.2 ± 4.7% RH), viability of L. minor decreasedrapidly, and no viability was observed after 120 min outside theaqueous medium (Fig. 4). In contrast, when exposed to moderatehumidity (66.9 ± 8.7% RH), viability was retained for a much longer

period (Fig. 4). Even colonies that had been out of the medium for6 h displayed some growth. We also found that under conditions ofhigh humidity (98.8 ± 1.4%) L. minor retained viability for in excessof 25 h. Extrapolating these survival data to the temperature andhumidity levels measured between the feathers of living birds(Fig. 2), survival for up to 6 h can be anticipated, especially incrissum and breast plumage. Survival within the crural and at thepostpatagium would potentially be longer. However, there is alsolikely to be increased risk of dislodgement at the postpatagiumduring flight, as well as changes in microclimate caused by venti-lation induced by wing beat.

Thus, mallard plumage can provide a suitable humid microcli-mate in which L. minor (an aquatic plant with limited capability toregulate transpiration) can potentially survive for extended periodsof time. At speeds of 65 km h�1 mallards easily cover long distancesand cross geographical barriers (Cabot, 1977). Yet, the conditions offlight, such as the effects of wind speed and wing beat on theplumage microclimate, need to be considered in more detail if weare to further our understanding of bird-mediated dispersal. Data-loggers attached to birds would make it possible to record micro-climatic conditions in flight. More examination of plumage micro-climatic conditions of bird species occupying contrasting ecologicalniches is also required. Nevertheless, together with the evidence ofentanglement and retention described by Coughlan et al. (2015),our measurements of microclimatic parameters make it likely thatmallards and other waterfowl contribute to dispersal of L. minor.Waterfowl are also likely dispersers of many other aquatic organ-isms. Known temperature and humidity regimes within theplumage microclimate, combined with known species desiccationtolerances, will allow dispersal kernel modellers to accuratelyassess dispersal distance and propagule survival. In a study byBarnes et al. (2013) aquatic plant species Elodea canadensis, Egeriadensa, Myriophyllum aquaticum, Myriophyllum heterophyllum, andPotamogeton richardsonii all retained viability after 3 h of desicca-tion exposure at 25 �C and 40 ± 8% RH (±SD). Mallard ducks couldpotentially relocate over 200 kmwithin a 3 h period. Van Leeuwenand van der Velde (2012) examined desiccation tolerance of 13common aquatic snail species. Almost all snail species survived48 h of desiccation at 10 and 20 �C under 80e85% RH. Based on theobserved microclimate data, mallard ducks could facilitate longdistance dispersal of the aforementioned species. This findingneeds to be considered in the context of the dispersal of invasivealien species, and their ecological management.

Acknowledgements

We gratefully acknowledge technical support from JohnCoughlan and Gavin O'Regan. We also would like to thank twoanonymous reviewers for helpful comments on an earlier draft.M.A.K.J. appreciates support by WoB.

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