RESEARCH PAPER

Nestedness in sessile and periphytic rotifercommunities: A meta-analysis

Phuripong Meksuwan1, Pornsilp Pholpunthin1, Elizabeth J. Walsh2, Hendrik Segers3 andRobert L. Wallace4

1Department of Biology, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, Thailand2Department of Biological Sciences, University of Texas at El Paso, El Paso, TX, USA3Belgian Biodiversity Platform, Royal Belgian Institute of Natural Sciences, Brussels, Belgium4Department of Biology, Ripon College, Ripon, WI, USA

The freshwater littoral comprises a mosaic of habitats structured at several scales by acombination of hydrophyte architecture and physiology. Within this complex environmentlittoral invertebrates should distribute themselves to maximize fitness: that is, for sessileanimals selection of permanent substrata is critical, while distribution of motile (periphytic)animals should follow predictions of Ideal Free Distribution theory. Here we explore therelationships between littoral rotifers and hydrophytes by conducting nestedness analyses on10 published datasets (7 sessile; 3 periphytic); one dataset each of microcrustaceans andinsects were included for comparison. We used four metrics to assess nestedness: meanmatrix temperature (T); counts of discrepancy shifts and species segregation; and percentsingletons. Six sessile rotifer datasets exhibited nestedness (T¼ 9.25–30.2°, supported by�2 null models; the other metrics varied widely). Our results indicate that distribution ofsessile rotifers and periphytic insects was highly structured, but until more data is availablelittle can be said about the distribution of the periphytic rotifer or microcrustacean communitystructure. Sessile rotifer species possessing idiosyncratic temperatures (T>T þ1.5 SD)exhibited a trend toward a record of cosmopolitanism. Important idiosyncratic hydrophytesincluded Ceratophyllum, Chara, and Utricularia. Two of the three periphytic, rotifer datasetsexhibited nestedness (T¼19.2°, 39.9°), but each was supported by only one of the four nullmodels. The periphytic microcrustaceans did not show nestedness, while the insects did(T¼ 15.5°; supported by four null models). The three other metrics varied considerably amongthe periphytic datasets, showing no discernable pattern.

Received: January 13, 2013Revised: September 3, 2013

Accepted: September 25, 2013

Keywords:Habitat dependent survival / Hydrophyte / Ideal free distribution theory / Nestednessanalysis / Substratum selection

1 Introduction

“Why does an animal live where it does?What is the nature of the ties that bind it to itsworld?”

— Rachel Carlson

Hydrophytes of the freshwater littoral have the capacityto alter their habitat in striking ways [1]. At the largest scale,they alter physical characteristics of the water column byslowing water movement thus increasing sedimentation

Correspondence: Dr. Robert L. Wallace, Department of Biology,Ripon College, Ripon, WI 54971, USAE-mail: wallacer@ripon.eduFax: þ1-920-748-7243Abbreviations: a, mean species richness per hydrophyte; bp,Beta proportional diversity; IFD, Ideal Free Distribution theory; S,species richness; T, mean matrix temperature

International Review of Hydrobiology 2014, 99, 1–10 DOI 10.1002/iroh.201301703

© 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1

and by reducing light penetration, which in turn keepswater temperature lower and may affect oxygen levels [2–4]. At intermediate scales, hydrophytes modify waterchemistry by altering pH, and changing concentrations ofcompounds important to plant physiology (e.g., inorganiccarbon, nitrogen, and phosphorus), as well as changinglevels of O2 and dissolved organic carbon [5–7]. Aroundindividual plants, small-scale effects dominate. Herehydrophyte architecture modifies water flow among thefoliage [8, 9] and provides structural complexity [10–12]that can conceal predators and prey from one another [13–15]. Also at this scale, plant physiology can markedly alterwater chemistry within the Prandtl boundary: the thin layerin the immediate vicinity of the plant in which all flow islaminar [16, 17]. Accordingly, the freshwater littoral shouldbe recognized as a mosaic of distinct habitats whosestructure and function depend on hydrophyte density anddiversity. As a result, fitness of littoral rotifers will bedetermined, in part, by the dominant hydrophytes in thehabitat.

A sessile (epiphytic) rotifer becomes bound to itssubstratum when the mobile juvenile (larva) encounters asurface and undergoes metamorphosis that ends inpermanent attachment. Consequently, while habitat-de-pendent survival and subsequent reproduction determinesfitness, the outcome is initiated by the act of substratumselection [18–20]. On the other hand, periphytic speciesare motile as adults and can move among hydrophytes,and of course they also may be residents of open waters.For example reporting on hydrophyte dominated waters ofthe Yamuna River (India) Arora and Mehra [21] haveshown that of the 90 motile rotifers present, 57 wereperiphytic (found in association with Eichhornia and/orSalvinia) and 48 were both pelagic and periphytic. Yetthere are some characteristics that set periphytic speciesapart from those that are truly pelagic. While not attachedto a specific plant, periphytic rotifers occur near enough tohydrophytes to be exposed to a distinct milieu, many feedwithin the aufwuchs, and some species deposit their eggson plants or at least release them within the littoralzone [13, 22–24]. For those species that deposit their eggson hydrophytes fitness of the embryo is determined insimilar ways as for sessile taxa. However, as mobileadults, periphytic species should distribute themselvesaccording to Ideal Free Distribution (IFD) theory: that is,fitness is maximized by exploiting the available habitatsbased on the aggregate of positive (e.g., resources) andnegative (e.g., predators) assets associated with each [25].Unfortunately, we know almost nothing about the relativefitness of either sessile or periphytic rotifers as a function oftheir habitat [20, 26].

While the species richness [27] and abundance [28] inthe littoral rotifer community appears to be as least asgreat, and often greater, than that of open waters [29]

(cf. [30]), these taxa remain an understudied component ofaquatic systems. Here we present a retrospective analysisof sessile and periphytic rotifer community structure vianestedness analysis, using datasets on littoral micro-crustaceans and insects for comparative purposes.Recognizing differences in diversity and composition ofthe littoral rotifer community offers us opportunity tounderstand the importance of the hydrophytes in structur-ing this habitat.

2 Methods

We compiled 12 published datasets (Table 1) of sufficientdetail that listed sessile or periphytic invertebrates that hadassociations with hydrophytes: sessile rotifers (n¼7),periphytic rotifers (n¼3), periphytic microcrustaceans(n¼ 1), and periphytic insects (n¼1). For simplicity werefer to these species as colonists; in this context the termcolonist should not be confused with colony, as in colonialrotifers (e.g., Floscularia conifera). These are species thatform intra- and interspecific aggregates by attaching to oneanother [31]. In our analysis we included colonial rotifers,but only in those instances of their being attached directlyto a hydrophyte. Of course, our study cannot beconsidered exhaustive, neither in the literature we selectednor in the thoroughness of each study (e.g., in parity ofplant surface area examined). For the rotifers we alteredspecies designations to conform to recent efforts tostabilize rotifer nomenclature [32, 33].

In our analysis we tested the hypothesis that colonistsof hydrophytes exhibited nestedness. In this case,nestedness indicates that colonists comprising smallerspecies assemblages on some hydrophytes are a nestedsubset of those hydrophytes with larger assemblages. Wedeveloped an initial data matrix comprising presence–absence data of S rows of rotifers and H columns ofhydrophytes. The matrix is rearranged (packed) usingalgorithms so that it achieves the densest grouping of SandH [34, 35]. While at least 10 metrics have been used toassess whether species assemblages exhibit nested-ness [36], we simplified our analyses by using fournestedness metrics. (1) Matrix temperature (T) is ameasure of disorder in a data matrix ranging from perfectnestedness (T¼ 0°) to maximum disorder (T¼ 100°), withintermediate temperatures indicating a combination oforder and disorder of the species assemblage [37]. Tocalculate T of the packed matrix we used ANINHADO [38,39]. Using this application all datasets were tested againstfour null models with 1000 simulations for each null model:(a) species presences are randomized within columns; (b)species presences are randomized within rows; (c)presence in a cell is randomized within the wholematrix; (d) presences are assigned by a function

P. Meksuwan et al. International Review of Hydrobiology 2014, 99, 1–10

2 © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Tab

le1.

Sum

maryof

nested

ness

metric

sforda

tase

tsof

inve

rteb

rate

colonists(ses

sile

orpe

riphy

ticsp

ecies)

andtheirhy

drop

hytesa

)

Loca

tion;

Referen

ceb) ;

[#of

sitesin

thestud

y]

Biodive

rsity

c)

#of

hydrop

hytes

Mea

nmatrix

T(#

ofnu

llmod

elsu

pport)d)

Discrep

ancy

shifts

(colon

ists;

hydrop

hytes)

Spe

cies

segreg

ation

Singleton

s(%

)

Idiosync

ratic

spec

iese

)

S,a,bp

Colon

ists

Hyd

roph

yte

Ses

sile

rotifers

A.Eight

states

,USA[194

]33

,16

.4,2.0

9f)

21.2°(4)

33;27

103(9.1%)

Collothec

aca

mpa

nulata;

Limnias

shiawas

seen

sis;

Ptygu

ramuc

icola

Roo

tedplan

tswith

large,

flat,

floatingleav

esB.Twostates

,USA

28,12

.4,2.3

8g)

23.2°(4)

21;21

107(35.7%

)Collothec

aca

mpa

nulata;

Cup

elop

agis

vorax;

Floscularia

ringe

ns;

Limnias

shiawas

seen

sis

Cha

ra

C.Pon

ds,German

y[22]

15,4.1,

3.6

1715

.8°(4)

26;22

84(26.7%

)Ptygu

rabrac

hiata

Algae

,Utricularia

sp.

D.Bog

pond

,NH,

USA[1]

19,8.6,

2.1

730

.2°(2)

17;15

26(31.6%

)Bea

ucha

mpiacruc

igera;

Ptygu

raba

rbata

Utricularia

gibb

a

E.Bog

s,German

y[10]

13,4.0,

3.3

79.5°

(3)

6;7

74(30.8%

)Bea

ucha

mpiacruc

igera;

Ptygu

ralong

icornis

Utricularia

interm

edia

F.Bog

san

dlake

s,Franc

e[7]

14,–

938

.4°(0)

NA

NA

2(14.3%

)–

–

G.Tha

leNoi

Lake

,Tha

iland

[1]

40,12

.3,3.3

1512

.3°(4)

47;50

1611

(27.5%

)Acyclus

sp.;Collothec

ahe

ptab

rach

iata;

Limnias

ceratoph

ylli

Ceratop

hyllum

demersu

m;

Utricularia

aurea

Periphy

ticrotifers

H.La

keKisajno

,Polan

d[4]

99,31

.2,3.2

4f)

39.9°(1)

33;32

1328

(28.3)

Con

ochilusna

tans

;Eos

phorana

jas;

Syn

chae

talong

ipes

;Syn

chae

tastylata;

Tric

hoce

rcaca

pucina

;Tric

hoce

rcaelon

gata;

Tric

hoce

rcastylata

–

I.Alıç

pond

,Turke

y[1]

60,21

.3,0.6

419

.2°(1)

10;17

74(6.7%)

Leca

nena

na;

Mon

ommatasp

.;Sca

ridium

sp.;

Tric

hoce

rcaob

tuside

ns;

Tric

hoce

rcarattu

s

Typ

hasp

.

(con

tinue

d)

International Review of Hydrobiology 2014, 99, 1–10 Sessile and periphytic rotifers

© 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 3

Table1.

(Con

tinue

d)

Loca

tion;

Referen

ceb) ;

[#of

sitesin

thestud

y]

Biodive

rsity

c)

#of

hydrop

hytes

Mea

nmatrix

T(#

ofnu

llmod

elsu

pport)d)

Discrep

ancy

shifts

(colon

ists;

hydrop

hytes)

Spe

cies

segreg

ation

Singleton

s(%

)

Idiosync

ratic

spec

iese

)

S,a,bp

Colon

ists

Hyd

roph

yte

J.Fores

tpo

nds,

Polan

d[7]

17,–

1044

.7°(0)

NA

NA

8(47.1%

)–

–

Periphy

ticmicrocrus

tace

ans

K.Alıç

pond

,Turke

y[1]

27,–

439

.7°(0)

NA

NA

0%–

–

Aqu

atic

inse

cts

L.Strea

msan

dlake

sMI,USA[16]

32,7.1,

4.5

1515

.5°(4)

40;38

1011

(34.4%

)Fou

rinse

ctsp

p.Potam

ogeton

alpinu

s,P.na

tans

,P.pe

ctinatus

Nes

tedn

essmetric

safterUlrich

[37].

a)Hereweex

pand

edthede

finitio

nof

hydrop

hyte

toinclud

efilamen

tous

alga

e,as

wella

sbo

thva

scular

andlarge,

non-va

scular

plan

ts.

b)A.T

able9[66];B

.sub

seto

fA(pg49

–50

);C.T

ext[80

];D.T

able2,

[18]

with

additio

nalunp

ublishe

dda

ta;E

.Tex

t[81

];F.T

able1[82];G

.Tab

le2[65];H

.Tab

leVIII

[83];

I.&K.Tab

le1[84];J.

Tab

le4[70];L.

Tab

le2[85].

c)S¼sp

eciesric

hnes

sof

thesite

(¼gdive

rsity)a

ndforp

acke

dmatric

eswith

atleas

t1nu

llmod

elsu

pport:a¼mea

nSpe

rhyd

roph

yte,

bp¼bprop

ortio

naldiversity(g/a).

d)Sup

port(p<0.05

)by

employ

ingatest

offour

nullmod

elsas

describ

edin

Sec

tion2of

[39].

e)Idiosync

rasy

forc

olon

ists(m

icrocrus

tace

ans,inse

cts,or

rotifers)

andtheira

ssoc

iatedhy

drop

hyteswas

define

das

thos

ewith

individu

alT¼themea

nmatrix

Tþ1

SD

(see

Sec

tion2).

f)Sub

strata

weregrou

pedinto

catego

ries,

notsp

ecies.

g)Rotife

rsattach

edto

ase

lect

grou

pof

hydrop

hyte

gene

ra.

P. Meksuwan et al. International Review of Hydrobiology 2014, 99, 1–10

4 © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

((Pi /c)þ (Pj /R))/2, where Pi is the number of presences inrow i, Pj is the number of presences in column j, R is thenumber of rows, and C is the number of columns [39].Simulation outputs from the four null models were testedusing a Permutation Hypothesis Test, with a<0.05. Wearbitrarily defined idiosyncratic species (both colonists andhydrophytes) as having an individual T that was greaterthan the meanmatrix Tþ1.5 SD. (2) In a packed matrix themetric termed Discrepancy shifts designates the totalnumber of moves of unexplained presences (outliers)needed to fill unexplained absences (holes) that thenresults in a filled matrix. (3) Species segregation (anti-nestedness or checkerboards) is the number of speciesoccurrences showing reciprocal exclusions in a 2� 2 sub-matrix [40]. (4) Spatial turnover or percent singletons is thenumber of taxa associated with only one hydrophyte,potentially indicating extreme specificity [37, 41] or merelyrarity. Of course, inadequate sampling also may accountfor the occurrence of singletons.

3 Results

3.1 Sessile rotifers

Of the seven sessile rotifers datasets analyzed, sixdemonstrated nestedness (T¼ 9.5–30.2°) with supportfrom at least two null models (Table 1). In the six datasets atotal of 56 taxa, representing �49% of sessile species(Collothecaceae¼ 17; Flosculariaceae¼ 39) listed by [32]were present. Their species richness (S) and mean S perhydrophyte (a) varied widely, 13–40 and 4.0–16.4,respectively, while b proportional diversity (bp), an indexof the difference in species composition among allhydrophytes in a habitat (bp¼S/a), ranged from 2.0 to3.6. In the nested habitats this means that smallerassemblages of species comprised non-random, nestedsubsets of those on hydrophytes with larger sessilecommunities. In the absence of nestedness, sessilespecies would be assembled randomly on the availablehydrophytes.

The best example of a nested dataset is that of ThaleNoi Lake, with S¼ 40 (12 genera). In the packed matrix(Fig. 1), each filled square indicates that a species wasobserved on a hydrophyte. The open circle is the inflectionpoint that delineates the approximate position of the matrixisocline of perfect nestedness (dashed line) [37]. In aperfectly nested situation, all interactions would lie abovethe isocline (i.e., to the upper left of the isocline) and nonebelow. While this dataset (Table 1, row G) has a matrix T of12.3° supported by 4 null models (p<0.05), there are alarge number of discrepancy shifts in both colonists(n¼ 47) and hydrophytes (n¼ 50). There were 16reciprocal exclusions of species in the packed matrix. Of

these, 12 pairings were within a feeding guild: that is, bothspecies were raptorial or both microphagous [42]. Theremaining four pairs were exclusions that crossed guildlines: for example, Stephanoceros fimbriatus (raptorial) v.Ptygura wilsonii (microphagous).

Figure 1. Plant–sessile rotifer interaction as illustrated in anestedness matrix for the data set of sessile rotifers fromThale Noi Lake, Thailand [65] (Table 1, row G). Numbersbeneath the hydrophytes are the total number of sessiletaxa found on a hydrophyte (i.e., hydrophyte a diversity)and the numbers to the left of the rotifer species names arethe total number of times the taxon was recorded on a plantin this study. In this study habitat g diversity was 40. Opencircle¼ inflection point; dashed line¼approximate posi-tion of the matrix isocline of perfect nestedness.

International Review of Hydrobiology 2014, 99, 1–10 Sessile and periphytic rotifers

© 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 5

As illustrated by the high number of singletons (n¼ 11,i.e., 27.5% of the species pool), this assemblage alsoshowed high spatial turnover. These changes in commu-nity structure – seen in the progressive decrease in sessilecolonists (i.e., left to right in Fig. 1) – probably reflectspecies responses to substantial differences in theenvironment created by the various hydrophyte species.However, these taxa showed no obvious pattern in theirfeeding type (e.g., 6 microphagous vs. 5 raptorial species).Three rotifers had high idiosyncratic T (Acyclus sp.,Collotheca heptabrachiata, and Limnias ceratophylli),but there appears to be no distinguishing commoncharacteristic among these taxa (e.g., presence of, orcomposition of a tube; feeding type). Two idiosyncratichydrophytes (Ceratophyllum demersum and Utriculariaaurea) comprised 24% of the discrepancy shifts. Bothspecies possess highly divided leaves and members ofboth genera are know to alter the chemistry immediatelysurrounding their leaves: Ceratophyllum produces pHdifferences between upper and lower leaf surfaces [43,44]; Utricularia uses a positive feedback loop of nutrientuptake and release that increases epiphytic growth ofalgae [45]. Three hydrophytes were species poor:Eleocharis ochrostachys (n¼ 1), Nymphoides indicum(n¼ 2), and Potamogeton malaianus (n¼ 3). We see noobvious traits that may account for this commonality.

Of the remaining six datasets, five showed nestednesssupported by at least two null models; the T values rangedfrom 9.5 to 30.2°, with 1–4 rotifers and 1–3 hydrophytespossessing idiosyncratic T values. Discrepancy shifts forboth colonists (6–33) and hydrophytes (7–27) and speciessegregation values (2–10) were all lower than what wasseen in Thale Noi Lake (16). Except one dataset (Table 1row A), the percent singletons found in these other studiesabout the same as in Thale Noi Lake. In generalhydrophytes fell into two groups: (1) species poor – forexample, Chara, filamentous algae, and rooted plants withlarge, flat, floating leaves and (2) species rich – forexample, Ceratophyllum, Myriophyllum, Potamogeton,and Utricularia.

3.2 Periphytic rotifers and periphyticmicrocrustaceans and periphytic insects

Two of three studies examined periphytic rotifers demon-strated nestedness (T¼ 39.9°, 19.2°), but support for inboth was limited to a single null model (Table 1). Of these, atotal of 125 species were recorded, more than twice therichness of the sessile datasets. For these two datasets Sand a were high, 60–99 and 21.3–31.2, respectively; bpdiffered widely: 0.6 and 3.2.

For the dataset from a pond in Turkey (Table 1, row I)discrepancy shifts for the rotifers (10) and hydrophytes(17), as well as species segregation values (7) were in the

same range as seen in the sessile assemblages. Thepercent singleton value (6.7%) was the lowest of alldatasets examined. However, these parameters weremuch higher for the dataset from Lake Kisajno (Poland),perhaps due to the fact that the hydrophytes were groupedinto broad categories (Table 1, row H).

Only one dataset of periphytic microcrustaceans wasexamined, but it did not exhibit nestedness (Table 1, rowK). The dataset of aquatic insects (n¼ 32) colonizing 15species of Potamogeton (Table 1, row L) exhibitednestedness (T¼ 15.5°; supported by 4 null models) witha high level of discrepancy (40 and 38, respectively),species segregation (10), and singletons (n¼ 32; 34.4%).

4 Discussion

Although nestedness analysis has been applied toplanktonic [46] and periphytic [47] rotifer communities, toour knowledge this is the first application of nestednessanalysis to sessile rotifer communities.

Hydrophytes provide habitat for both mobile and sessileinvertebrates, but they alter the physical and chemicalproperties of their immediate surroundings in complexways and their associated invertebrates respond to thesedifferences. These plants represent islands: that is,resource patches potentially providing suitable habitat,food sources, and refugia. In island biogeographic theory,degree of isolation (distance from source populations) andhabitat size are critical factors in determining speciesrichness. In the freshwater littoral, degree of isolation isprobably inconsequential at two levels: swamping effectsfrom hatching diapausing embryos and proximity of otherplants. However, plant surface (including spatial architec-ture) is known to be important for both sessile andperiphytic rotifers: flat surfaces in Cupelopagis vorax [48,49] and plant structural complexity in Euchlanis dila-tata [13]. Structural complexity also is important for littoralmicrocrustaceans: (e.g., [50]). While Hann [51] has shownthat plant biomass (an approximation for surface area) tobe an important factor in accounting for mean number ofperiphytic rotifers, it was insufficient to account for their lowdensity on Chara. Our own unpublished observationssupport the idea that Chara is relative poor habitat forrotifers in Chihuahuan desert systems. On the other hand,working in a shallow, hydrophyte-dominated lake inPoland, Kuczyńska-Kippen and Nagengast [29] reportbiodiversity values (H0) for rotifers associated with twospecies of Chara (2.46 and 2.61). These values werehigher than that for Nymphaea alba (2.36), Utriculariavulgaris (2.36), and open water (1.46), but not Myriophyl-lum verticillatum (2.74). Rotifer diversity also can varywithin a stand of hydrophytes. In her analysis of rotiferscollected from two regions (central vs. edge) of a bed of

P. Meksuwan et al. International Review of Hydrobiology 2014, 99, 1–10

6 © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Myriophyllum verticillatum, Kuczyńska-Kippen [52]reported seven taxa with significantly greater density inthe Myriophyllum bed, but only a single species waspresent in the edge region.

One area that still has not received sufficient attention isthe effect that allelochemicals released by hydrophyteshave on rotifers [53] and other zooplankton [54]. We doknow that factors associated with specific hydrophytesinfluence habitat choice by both sessile and periphyticrotifers. Moreover, several studies suggest that hydrophyteallelochemicals have a negative influence on epi-phytes [55–58]. Thus, while surface area and structuralcomplexity are important variables hydrophytes are notfungible with an equivalent surface area of an inert object.Following are three examples. (1) Utricularia is known forits species richness in sessile rotifers [26, 59], with Ptygurabeauchampi exhibiting an extreme preference for one offive species of this carnivorous plant [60]. (2) JuvenileCollotheca (gracilipes) campanulata preferentially settleon the under surfaces of Elodea canadensis leaves basedchemistry of the Prandtl boundary [20]. (3) The motilespecies Euchlanis dilatata exhibits an example of habitatloyalty in oviposition in which females laid more eggs onthe hydrophyte from which they had been collected(Myriophyllum exalbescens) than on two other hydro-phytes [22]. Moreover this preference persisted even aftertwo generations in culture without contact with Myriophyl-lum. In this regard more attention should be given to theincidences of singleton species (Fig. 1; Table 1). Whilesingletons may simply be records of rare occurrences ofsingle specimens, large numbers of specimens inassociation with one hydrophyte could indicate strongsubstratum selection (e.g., P. beauchampi [61]) and/orhabitat dependent survival in sessile species. Periphyticrotifers having singleton associations with hydrophytesmay indicate that the animals distribute themselvesaccording to the predictions of IFD theory. For example,in experimental tanks Brachionus plicatilis congregated ina thin layer of Nannochloropsis oculata only to disperseafter depletion of the algae [62].

Another aspect of the colonization of plants by sessilerotifers that has not been explored is the ultrastructuraldetails of the epidermal surfaces of hydrophytes. Someplants are known to have anti-adhesive surfaces makingthem water repellent and self-cleaning; this phenomenonis known as the Lotus effect [63, 64]. Of the 14 generainvestigated by Meksuwan et al. [65] four are know topossess water pepellent surfaces [63]. We suggest thatthe anti-fouling potential of hydrophytes in limiting theability of sessile rotifers to colonize plants should beinvestigated.

Despite high rotifer biodiversity in habitats with exten-sive hydrophyte communities [15, 24, 29, 66–70] and theprobability that additional study will provide insight into

community structure, the littoral rotifer community has notreceived sufficient attention. Regrettably, most studieshave not reported information about rotifer-hydrophyteassociations in sufficient detail to gage what features ofthe plants are important to the rotifers; moreover, fewstudies have examined both the sessile and periphyticcommunities simultaneously. Such investigations arerequired for a more complete understanding of theecological processes of rotifer distribution in this distincthabitat. A logical approach would be to focus on twofronts: field and laboratory. In the field concurrentsampling of both the sessile and periphytic taxa iswarranted. Samplers that simultaneously capture bothfauna have been described; these include trappingcontainer samplers [51, 71–76], jar covering meth-ods [77], or syringe samplers [78] followed by grabbingthe hydrophyte. The use of artificial substrata [48, 79]and common garden experiments [50] in both field andlaboratory studies (i.e., microcosms) will provide a morecontrolled way to gather information on the importanceof physical structure v. plant physiology in the estab-lishment of nested assemblages. By using the researchapproaches outlined here we should be able toelucidate the importance of the physical and chemicalmilieu immediately surrounding different plants instructuring the sessile–periphytic community.

We thank Tim Hess, who aided us in the statisticalanalysis, and Hilary A. Smith and two anonymousreviewers who read and improved our manuscript. Thisresearch is based upon work partially supported by theNational Science Foundation under BSR #8405157 andDEB #0516032, National Center for Research Resources(NCRR), a component of the National Institutes of Health(NIH) Grant Number 5G12RR008124, and Funds forFaculty Development (Ripon College). The contents aresolely the responsibility of the authors and do notnecessarily represent the official views of NSF or NIH.

The authors have declared no conflict of interest.

5 References

[1] Špoljar, M., Fressl, J., Dražina, T., Meseljević, M., Grčić, Z.,Epiphytic metazoans on emergent macrophytes in oxbowlakes of the Krapina River, Croatia: Differences related toplant species and limnological conditions. Acta Bot. Croat.2012, 71, 125–138.

[2] Carpenter, S. R., Lodge, D. M., Effects of submergedmacrophytes on ecosystem processes. Aquat. Bot. 1986, 26,341–370.

[3] Madsen, J. D., Chambers, P. A., James, W. F., Koch, E. W.,Westlake, D. F., The interaction between water movement,sediment dynamics and submersed macrophytes. Hydro-biologia 2001, 444, 71–84.

International Review of Hydrobiology 2014, 99, 1–10 Sessile and periphytic rotifers

© 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 7

[4] Fontanarrosa, M. S., Chaparro, G., de Tezanos Pinto, P.,Rodriguez, P., O’Farrell, I., Zooplankton response to shadingeffects of free-floating plants in shallow warm temperatelakes: A field mesocosm experiment. Hydrobiologia 2010,646, 231–242.

[5] Banoub, M. W., The effect of reeds on the water chemistry ofGnadensee (Bodensee). Arch. Hydrobiol. 1975, 75, 500–521.

[6] Frodge, J. D., Thomas, G. L., Pauley, G. B., Effects of canopyformation by floating and submergent aquatic macrophyteson the water quality of two shallow Pacific Northwest lakes.Aquat. Bot. 1990, 38, 231–248.

[7] Arora, J., Mehra, N. K., Seasonal dynamics of rotifers inrelation to physical and chemical conditions of the riverYamuna (Delhi), India. Hydrobiologia 2003, 491, 101–109.

[8] Hutchinson, G. E., A Treatise on Limnology, Volume III,Limnological Botany, John Wiley & Sons, New York 1975.

[9] Khublaryan, M. G., Frolov, A. P., Zyryanov, V. N., Modelingwater flow in the presence of higher vegetation. Water Res.2004, 31, 617–622.

[10] Taniguchi, H., Nakano, S., Tokeshi, M., Influences of habitatcomplexity on the diversity and abundance of epiphyticinvertebrates on plants. Freshwater Biol. 2003, 48, 718–728.

[11] Hansen, J. P., Sagerman, J., Wikström, S. A., Effects of plantmorphology on small-scale distribution of invertebrates.Mar.Biol. 2010, 157, 2143–2155.

[12] Hansen, J. P., Wikström, S. A., Axemar, H., Kautsky, L.,Distribution differences and active habitat choices ofinvertebrates between macrophytes of different morphologi-cal complexity. Aquat. Ecol. 2010, 45, 11–22.

[13] Walsh, E. J., Habitat-specific predation susceptibilities of alittoral rotifer to two invertebrate predators. Hydrobiologia1995, 313/314, 205–211.

[14] Bowszys, M., Hirsz, E., Paturej, E., The role of macrophytesin the diurnal distribution of crustacean zooplankton in alittoral of a shallow, macrophyte-dominated lake. Electron. J.Pol. Agric. Univ. Biol. 2006, 9, 18.

[15] Kuczyńska-Kippen, N., Habitat choice in rotifera communi-ties of three shallow lakes: Impact of macrophyte substratumand season. Hydrobiologia 2007, 593, 27–37.

[16] Lucas, W. J., Photosynthetic assimilation of exogenous HCO3�

by aquatic plants. Annu. Rev. Plant Phys. 1983, 34, 71–104.

[17] Borowitzka, M. A., Calcification in aquatic plants. Plant CellEnviron. 1984, 7, 457–466.

[18] Wallace, R. L., Distribution of sessile rotifers in an acid bogpond. Arch. Hydrobiol. 1977, 79, 478–505.

[19] Wallace, R. L., Ecology of sessile rotifers. Hydrobiologia1980, 73, 181–193.

[20] Wallace, R. L., Edmondson, W. T., Mechanism and adaptivesignificance of substrate selection by a sessile rotifer.Ecology 1986, 67, 314–323.

[21] Arora, J., Mehra, N. K., Species diversity of planktonic andepiphytic rotifers in the backwaters of the Delhi segment ofthe Yamuna River, with remarks on new records from India.Zool. Stud. 2003, 42, 239–247.

[22] Walsh, E. J., Oviposition behavior of the littoral rotiferEuchlanis dilatata. Hydrobiologia 1989, 186/187, 157–161.

[23] Duggan, I. C., Green, J. D., Thompson, K., Shiel, R. J.,Rotifers in relation to littoral ecotone structure in LakeRotomanuka, North Island, New Zealand. Hydrobiologia1998, 387/388, 179–197.

[24] Duggan, I. C., The ecology of periphytic rotifers. Hydro-biologia 2001, 446/447, 139–148.

[25] van der Hammen, T., Montserrat, M., Sabelis, M. W., deRoos, A. M., Janssen, A.,Whether ideal free or not, predatorymites distribute so as to maximize reproduction. Oecologia2011, 169, 95–104.

[26] Edmondson, W. T., Ecological studies of sessile Rotatoria,Part II. Dynamics of populations and social structure. Ecol.Monogr. 1945, 15, 141–172.

[27] Pennak, R. W., Structure of zooplankton populations in thelittoral macrophyte zone of someColorado Lakes.Trans. Am.Microsc. Soc. 1966, 85, 329–349.

[28] Stefanidis, K., Papastergiadou, E., Influence of hydro-phyte abundance on the spatial distribution of zooplanktonin selected lakes in Greece. Hydrobiologia 2010, 656, 55–65.

[29] Kuczyńska-Kippen, N. M., Nagengast, B., The influence ofthe spatial structure of hydromacrophytes and differentiatinghabitat on the structure of rotifer and cladoceran communi-ties. Hydrobiologia 2006, 559, 203–212.

[30] Pejler, B., Relation to habitat in rotifers. Hydrobiologia 1995,313/314, 267–278.

[31] Wallace, R. L., Coloniality in the phylum Rotifera. Hydro-biologia 1987, 147, 141–155.

[32] Segers, H., Annotated checklist of the rotifers (PhylumRotifera), with notes on nomenclature, taxonomy anddistribution. Zootaxa 2007, 1564, 1–104.

[33] Segers, H., De Smet, W. H., Fischer, C., Fontaneto, D., et al.Towards a list of available names in zoology, partim phylumRotifera. Zootaxa 2012, 3179, 61–68.

[34] Fontaneto, D., Ficetola, G. F., Ambrosini, R., Ricci, C.,Patterns of diversity in microscopic animals: Are theycomparable to those in protists or in larger animals? GlobalEcol. Biogeogr. 2006, 15, 153–162.

[35] Ulrich, W., Gotelli, N. J., Null model analysis of speciesnestedness patterns. Ecology 2007, 88, 1824–1831.

[36] Ulrich, W., Almeida-Neto, M., Gotelli, N. J., A consumer’sguide to nestedness analysis. Oikos 2009, 118, 3–17.

[37] Ulrich, W., Nestedness analysis as a tool to identifyecological gradients. Ecol. Questions 2009, 9, 27–34.

[38] Atmar, W., Patterson, B. D., The measure of order anddisorder in the distribution of species in fragmented habitat.Oecologia 1993, 96, 373–382.

[39] Guimarães, P. R., Jr., Guimarães, P., Improving theanalyses of nestedness for large sets of matrices. Environ.Modell. Softw. 2006, 21, 1512–1513.

[40] Almeida-Neto, M., Guimarães, P., Guimarães, P. R. Jr.,Loyola, R. D., Ulrich, W., A consistent metric for nestednessanalysis in ecological systems: Reconciling concept andmeasurement. Oikos 2008, 117, 1227–1239.

[41] Baselga, A., Partitioning the turnover and nestednesscomponents of beta diversity. Global Ecol. Biogeogr. 2010,19, 134–143.

[42] Obertegger, U., Smith, H. A., Flaim, G., Wallace, R. L., Usingthe guild ratio to characterize pelagic rotifer communities.Hydrobiologia 2011, 662, 157–162.

[43] Prins, H. B. A., Snel, J. F. H., Helder, R. J., Zanstra, P. E.,Photosynthetic HCO3

� utilization and OH� excretion inaquatic angiosperms. Plant Phys. 1980, 66, 818–822.

[44] Prins, H. B. A., Snel, J. F. H., Zanstra, P. E., Helder, R. J., Themechanism of biocarbonate assimilation by the polar leaves

P. Meksuwan et al. International Review of Hydrobiology 2014, 99, 1–10

8 © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

of Potamogeton and Elodea. CO2 concentrations at the leafsurface. Plant Cell Environ. 1982, 5, 207–214.

[45] Ulanowizc, R. E., Utricularia’s secret: The advantage ofpositive feedback in oligotrophic environments. Ecol. Model.1995, 79, 49–57.

[46] Ramos-Jiliberto, R., Oyanedel, J. P., Vega-Retter, C.,Valdovinos, F. S., Nested structure of plankton communitiesfrom Chilean freshwaters. Limnologica 2009, 39, 319–324.

[47] Fontaneto, D., Melone, G., Ricci, C., Connectivity andnestedness of the meta-community structure of mossdwelling bdelloid rotifers along a stream. Hydrobiologia2005, 542, 131–136.

[48] Butler, N. M., Substrate selection and larval settlement byCupelopagis vorax. Hydrobiologia 1983, 104, 317–323.

[49] Bevington, D., White, C., Wallace, R. L., Predatorybehaviors of Cupelopagis vorax (Rotifera, Collothecacea;Atrochidae) on protozoan prey. Hydrobiologia 1995, 313/314, 213–217.

[50] Meerhoff, M., Iglesias, C., De Mello, F. T., Clemente, J. M.,et al. Effects of habitat complexity on community structureand predator avoidance behaviour of littoral zooplankton intemperate versus subtropical shallow lakes. Freshwater Biol.2007, 52, 1009–1021.

[51] Hann, B. J., Invertebrate associations with submersedaquatic plants in a prairie wetland. UFS (Delta Marsh)Ann. Rep. 1995, 30, 78–84.

[52] Kuczyńska-Kippen, N., The distribution of rotifers (Rotifera)within a single Myriophyllum bed. Hydrobiologia 2003, 506–509, 327–331.

[53] Hasler, A. D., Jones, E., Demonstration of the antagonisticaction of large aquatic plants on algae and rotifers. Ecology1949, 30, 359–364.

[54] Linde’n, E., Lehtiniemi, M., The lethal and sublethal effects ofthe aquatic macrophyte Myriophyllum spicatum on Balticlittoral planktivores. Limnol. Oceanogr. 2005, 50, 405–411.

[55] van Donk, E., van de Bund, W. J., Impact of submergedmacrophytes including charophytes on phyto- and zooplank-ton communities: Allelopathy versus other mechanisms.Aquat. Bot. 2002, 72, 261–274.

[56] Erhard, D., Gross, E. M., Allelopathic activity of Elodeacanadensis and Elodea nuttallii against epiphytes andphytoplankton. Aquat. Bot. 2006, 85, 203–211.

[57] Gross, E. M., Hilt, S., Lombardo, P., Mulderij, G., Searchingfor allelopathic effects of submerged macrophytes onphytoplankton – state of the art and open questions.Hydrobiologia 2007, 584, 77–88.

[58] Trochine, C., Modenutti, B. E., Balseiro, E. G., Chemicalsignals and habitat selection by three zooplankters in AndeanPatagonian ponds. Freshwater Biol. 2009, 54, 480–494.

[59] Segers, H., Meksuwan, P., Sanoamuang, L.-O., New recordsof sessile rotifers (Phylum Rotifera: Flosculariacea, Collo-thecacea) from Southeast Asia. Belg. J. Zool. 2010, 140,235–240.

[60] Wallace, R. L., Substrate discrimination by larvae of thesessile rotifer Ptygura beauchampi Edmondson. FreshwaterBiol. 1977, 7, 301–309.

[61] Wallace, R. L., Substrate selection by larvae of the sessilerotifer Ptygura beauchampi. Ecology 1978, 59, 221–227.

[62] Ignoffo, T. R., Bollens, S. M., Bochdansky, A. B., The effect ofthin layers on the vertical distribution of the rotifer Brachionusplicatilis. J. Exp. Mar. Biol. Ecol. 2005, 316, 167–181.

[63] Neinhuis, C., Barthlott, B., Characterization and distributionof water-repellent, self-cleaning plant surfaces. Ann. Bot.1997, 79, 667–677.

[64] Koch, K., Bohn, H. F., Barthlott, W., Hierarchically sculpturedplant surfaces and superhydrophobicity. Langmuir 2009, 25,14116–14120.

[65] Meksuwan, P., Pholpunthin, P., Segers, H., Diversity ofsessile rotifers (Gnesiotrocha, Monogononta, Rotifera) inThale Noi Lake, Thailand. Zootaxa 2011, 2997, 1–18.

[66] Edmondson, W. T., Ecological studies of sessile Rotatoria,Part I. Factors affecting distribution. Ecol. Monogr. 1944, 14,32–66.

[67] Basu, B. K., Kalff, K., Pinel-Alloul, B., The influence ofmacrophyte beds on plankton communities and their exportfrom fluvial lakes in the St Lawrence River. Freshwater Biol.2000, 45, 373–382.

[68] Kuczyn’ska-Kippen, N., On body size and habitat selection inrotifers in a macrophye-dominated lake Budzyn’skie, Poland.Aquat. Ecol. 2005, 39, 447–454.

[69] Sharma, B. K., Rotifer communities of floodplain lakes of theBrahmaputra basin of lower Assam (N.E. India): Biodiversi-ty, distribution and ecology. Hydrobiologia 2005, 533, 209–221.

[70] Basińska, A., Kuczyńska-Kippen, N., Differentiated macro-phyte types as a habitat for rotifers in small mid-forest waterbodies. Biologia 2009, 64, 1100–1107.

[71] Pennak, R. W., Quantitative zooplankton sampling in littoralvegetation areas. Limnol. Oceanogr. 1962, 7, 487–489.

[72] Minto, M. L., A sampling device for the invertebrate fauna ofaquatic vegetation. Freshwater Biol. 1977, 7, 425–430.

[73] Amoros, C., A simple device for quantitative pseudoper-iphyton sampling. Hydrobiologia 1980, 68, 243–246.

[74] Fairchild, G. W., Movement and microdistribution of Sidacrystallina and other littoral Microcrustacea. Ecology 1981,62, 1341–1352.

[75] Kornijów, R., Quantitative sampler for collecting invertebratesassociated with submersed and floating-leaved macro-phytes. Aquat. Ecol. 1998, 32, 241–244.

[76] Paggi, J. C., Mendoza, P. O., Debonis, C. J., José de Paggi,S. B., A simple and inexpensive trap-tube sampler forzooplankton collected in shallowwaters.Hydrobiologia 2001,464, 45–49.

[77] Sakuma, M., Hanazato, T., Nakazato, R., Haga, H., Methodsfor quantitative sampling of epiphytic microinvertebrates inlake vegetation. Limnology 2002, 3, 115–119.

[78] Pontin, R. M., Shiel, R. J., Periphytic rotifer communities of anAustralian seasonal floodplain pool. Hydrobiologia 1995,313/314, 63–67.

[79] Lucena-Moya, P., Duggan, I. C., Macrophyte architectureaffects the abundance and diversity of littoral microfauna.Aquat. Ecol. 2011, 45, 279–287.

[80] Tiefenbacher, L., Beträge zur Biologie und Ökologie sessilerRotatorien unter besonder Berücksichtigung des Gehäuse-baues und der Regenerationsfähigkeit. Arch. Hydrobiol.1972, 71, 31–78.

[81] Tiefenbacher, L., Zur Kenntnis sessiler Rotatorien desMurnauer Mooses in Oberbayern. Entomofauna 1982, 3,89–96.

[82] Francez, A.-J., Écologie des pluplements de rotifèressessiles des Lac-Tourbières D’auvergne (France). Bull.Ecol. 1984, 15, 213–237.

International Review of Hydrobiology 2014, 99, 1–10 Sessile and periphytic rotifers

© 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 9

[83] Klimowicz, H., Rotifers of “astatic waters.” Part I. The littoralof Lake Kisajno. Pol. Arch. Hydrobiol. 1964, 12, 278–305.

[84] Güher, H., Erdoğan, S., An investigation on the periphyticzooplankton species (Cladocera, Copepoda, Rotifera) in Alıç

pond (Turkey). J. Fisheries Sci. 2008, 2, 516–523 (In Turkish,with English abstract and figure legends).

[85] Berg, C. O., Limnological relations of insects to plants of thegenus Potamogeton. Trans. Am. Microsc. Soc. 1949, 68,279–291.

P. Meksuwan et al. International Review of Hydrobiology 2014, 99, 1–10

10 © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim