The systematics of the New Zealand species of Potamopyrgus (Mollusca: Hydrobiidae) and studies on the biology of Potamopyrgus antipodum : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Zoology at Massey University

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U·roLLU0CA

^: HYDHO:GIIDA:G:;), �4 ^...tlD dl'lJDIJi;0 01:-T :C.l:{r:; BIOLOGY OF :f·'O'l1.t\.IicOJ?Yi{G 1):3 Al·FCIFODUM

A ^thesis

presented Ln p�rtial fulfilment of the requirements for the

degree

^of

Doctor of Philosophy in Zoology at Dasscy University

foiiiCHASL JOl::IH WIN'l'.ERBOUHN

1968

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ABS'l'RACT

This investigation has shovm that only three suecies of Potamopyrgus Stimpson can be recognized. from New .6ealand,

compared with !;he six species and three subspecies recognized by Suter

(1913).

_The species are, P. sntinodum

Gray 184-3,

P. nunoid.es Hutton 1882, and P. cstuarinus n. sp. ^P. ^da.wbini Powell

1955

from the Auckland Islands is probably referable

to P. antiuodum, but the position of (?

)

^P. melvilli (Hedley

1916)

from the Kermadec Islands has not been determined. 'l'he European species P. ^jenkinsi

(S�ith 1889)

cannot be separated from P. antiuodum on morphological or anatomical grounds and may also �e referable to that species. All species �ow_

placed in Fluviouuoa Pilsbry

1911

should probably be referred

to

.Potarnouyrgus.

P. estuarinus and P. ouuoides are both smooth-shelled,

bisexual, non-ovoviviparous and confined to brackish water.

P. antioodum is

highly

variable in shell size,

shape

and ornamentation, inhabits fresh and brackish water, is_avovivi

parous, and populations may consist entirely

of partheno

genetic feillales, or contain variable numbers of sexually functional males. Rearing of snails in the laboratory ha s shown that snails do not necessarily breed true vrith respect to shell ornament?.�ion, .. and that shell shape and ornament

ation� is not determined prinarily by.environnental factors ^• ^. The shell of P. estuarinus cannot be distinguished from that .of some P. anti·oodum but P. uuuoides may be readily identified_ using shell characters alone. . l'To significant interspecific differences·in operculum,· external morphology,

]

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body

^p

i

^gm

en

^{tat i}

o

ⁿ

or

^s

t

^r

u

^c

t

^ur

e

^of the ^male

reproductive system are

.fOLmd

but

V.·

DUT)Oides

^possesses

minor

radular ^d

i

^f

fe

^ren^ces^,

and

^P. ^antiuodum differs in t11e concl.i tion

of

the ^female repro

d

^uc

t

ⁱ

v

^e

system . ., r.L'he

^d

i

^p

l

^oid

(2n) chrornosome number of all

three species

is 24.

��ualitative paper chromatography

^of ^crude

foot

^Tmscle

and

rnaqtle edge e

^xtracts, and quantitat ive ion-exchange cllrornato:�:raphy of

shell periostracal protein h

^a^ve ^disclosed no import

a

^nt

biochemical differences between

s

p e

ci

e s

.

F.

antiuoclum

^{i s}

widely distributed

in ^fresh

vmters

^and

no

clear

relationship

betveen shell

^shape and ornamenta t i on,

an

d different kinds of habitat hav

e

^{b een} ^found. P.

estuarinus

has a

fairly restricted

^brackⁱsh water habitat and

is

^fre

quently

^found ^near

river

^no

u

^ths ⁱⁿ

h

^a

r

bours

V'!here

^snails

may

r

e

gularly be exposed to the air

!

or part bf each t

i

^de ^{cyc l e.}

P.

u

uu^oⁱ

d

es is also restricted

to

^brackish

water but normally

r emains ful ly aquatic at

all times. Experimental studies on salinity

relationships,· hs.

b

^ita

t

s e l e c t io n

and the

effects of desⁱcca

t

i^on have demonstrated impor

t

^an

t

differences in. the

environmental

r' e latio nsh ips

o

^f

the·

^three

species

^which ^can ^be

c orrelated with the ir distributions.

J..Jife history

^and po:pulatiqn stucl,ies ma^de

in

^t^h

r

^{ee pop}

ulations of P.

antiuocl.um (tw()

^p

o

^nds ^and ^a

stream) over a 13- lL� month period have shown

that r eproduc t ion occurs thr

o

^ugh

out the y

e

^ar

with peak a

^c

t

^ivity ⁱⁿ

s

^pri

n

^g

and summer.

Gen

e

^rat^ion time as indicated by labo ratory

rearing of

^sna

il

^s

is

9-12

months. P^op

ul

atⁱoⁿ age

structures

^d

i

^ff

e

^r^ed ^{�ark edly}

between

^-ponds

and

str eam and reflect

e

^d differences in ^the

ll

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physical environments of the two habitats. Distribution, occurrence in drift and effects of floods were examined in the stream. Snails were generally rnost abundant in places sheltered from the main current or among vegetation, and

large numbers were present within n1ats of willmv roots. P.

antipodum is a regular member of the drift fauna and floods

have an

important role in regulating population age.structure.

The distribution of P. antinodum in thermal waters was also.investigated, and experimental work indicates that high water t�mperature is probably the most important factor limit

ing distribution.,. 'l'he, rnax�murn temperatv.re at which snails were found in the field,

28°(;,

is also the temperature at which activity"9ea�es and the snails enter.

a

co�atose state.

_Finally, .a study has. been made of the parasites of

Potamopyrgus. An ��ident�tied �rotozoan (�porozoa _:

Porosporidae

)

, occurring. in an en.cysted state, is the most ii;1portant internal parasite v1ith infection rates as high as

86%

having be�n rccordeq ^�

.

The la:rvae , of·

13

species of,.

Trematoda were identified and briefly described and their _.· _-· _� rates of infection determined. The-monostome cercariae are the most important group of parasitic trematodes ^•.^. 'l'he

commensal, oligochaete Chaeton:aster limnaei. limnaei was found in association with P. antiuodum in· .Lake Pupuke, Auckland, and was observed to be predacious on embryonic snails.

.J...J...J..

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PREFACE

A thoro1.1gh investigation of the

systematics

of the lTew lealand species of �otamooyrgus has long been overdue and is

the main ain of this thesis. Comoarative examinations of morphological, anatomical

and

biochemical factors, as well

as environmental relationships have been

made

ⁱⁿ ^the ^se^ar^ch

fof specⁱ^es differen ces and ⁱⁿ ^order ^to describe

the ext

ent of inter- and intraspecific variation r·i thin the component

s

pecies. All factors have �een examined primarily for any

systematic i

nf

^or

m

^ation

they

T'lay ^yield rather than to eluc

idate s·tructure and function for its own sake.

In the systemat ic section of thi s thesis the conclusions reached as a result of the study are presented before the detai led a c c ount of the investigations leading to their form

ulation. This has permitted a more cohe s ive account to be written with the emphasis being placed on interspecific differences.

The se condary aim of this work has been to examine some aspects of the biology of the freshwater species P. antipodum.

This has invol :.�red studies of the life histor

y

^and population dynamics in three populations, field and experimental work on thermal relations, and an ·examination of the snails' parasites and their rates of infection.

lV

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I ao pleased to acknowledge and thank those people viho b.ave assisted me during the course of this wor^k, in particular Dr. ^T.J. J3ro�.�m for his interest and criticism

throughout. The advice and criticism of Dr. W.C. Clark

and t:.r. L. ^{Gurr of} the Lioology Department, Niassey

University, and Dr. R.K. ^Dell

and Mr. �.F. Ponder of the

Dominion Museum, �ellinB^ton^, ^has also been greatly

appreciated, as has the help given by Dr.

G. G .

l>.!idwinter, Dep

a

rtment o f Chemistry and Biochemistry, Massey

University, with biochemical aⁿalyses, and rZiss Pauline Cam:9bell and Mr. D. Greenwood for teclmical assistance.

Dr. Dell and T·i�r. P^ond^er ^have kindly allovved me to examine material in the Dor1inion IJfuseum collections and have introduced me to much relevant literature.

Collections of snails have been made for me by Uessrs.

John ::!IcLean of 1\.uc1:land and lan r,�cLellan of Westport^.

�·r. ^To� ^i!a^rrJick of the University of Edinburgh has sent me living materia^l ^of ^P. ,j en...'kinsi, and T1rs. Shirley Pc)iind of the Zoology Department, University of Canterbury, has lent me trematode material. It gives me pleasure to acknowledge the help given by all these people.

All figures in this thesis were-reproduced by the

�1!assey U^niversity 1 Central Photographic Unit.

V

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1 . 42

1.44

2.0

BIOCHEMICAL :B'AC'rORS

Introduction j·.::ethods

Results and discussion

(a) T·.fucus fluorescence

(b)

Free amino acids

(c) Amino acids of periostracal protein ELITVIRONM.El'FrA:L RI!}LAT IONSHIPB

(a) Distribution and general ecology (b) Salinity relations

(c) Habitat preference

(d)

Desiccation DISCUSSION

(a) The species problem

(b) The significance of parthenogenesis (c) Shell ornamentation

(d) The relationship of Fluvionuua

Page

46 51

54 54 55

61 66 72 74

79 84 89

to Potamouyrgus

93

(e) The relationship of P. antinodum to the European species P.

.j

en_'l{:insi

BIOLOGICAL S�J:IODIE.S ON P. ANTIPODUM

95

2.1

POPULATION .S'rUDIES

Introduction

100

Study areas

101

Climate

102

Methods

106

Results and discussions

(a) Life history and population dynamics

111

(b) Stream ecology

127

·v11

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3 . 0

THERMAL RELNe!ONSHIPS OF' P. ANTIPODUM

Introduction

Materials-and methods Results

Discussion

4. 0

PARASITES OF POTAii�OPYH.GUS

5 . 0

Introduction Methods

Larval 'I'rematoda Protozoa

Oligochaeta

REFERENCES APPENDICES

' ' .

Page

134 134 137 139

140 140 141

156

158

160

183

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3. 0

THEill)JAL RELA�riONSHIPS OJJ' P. ANTlPODUM Introduction

Materials and methods Hesults

Discussion

4 . 0

PAI-tASrr.GS OF POTAl·.�OPYHGUS

5.0

Introduction Methods

Larval 'I'rematoda Protozoa

Oligochaeta REFE.R�NCES

APPENDICES

, · ··· - _{' '}

Page

134 134 137 139

140 140 141 156 158 160 183

Vlll

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IND:F.!:X TO FIGURES Figure

l .

Followinq; p::tg;e

2.

Measurements made in the study o f shell shape variation .

Shell he ight plotted against shell width, an.d aperture he ight in

:P.

anti podum .

3. Outline trac ings of fully-gro·wn smooth shell s 4.

of Potamonyrgus sp� .

Outline trac ings of fully- gro�m ornamented (spiny) shel l s of

P.

antinodum .

5. Shells of P. e stuarLrms and P . nuno ides , and

6.

perio strac�l ornamentation of P . antino dum . (a) It�aximum shell he ight in

populations

of Potamopyrgus spp .

(b) �:Tean he ight: width and hei?;ht: aperture he ight ratios in

P.

antiuodum.

7 . �ean shell hei�ht plotted �gainst mean

8.

height:ape rture he ight ratio , and against mean he ight:width ratio , in

P.

antipodum .

( a)

Whorl

diameters of embryonic shells of

P.

antiuodum

^•

. (b) Range of variation in shell he ight:she ll width , and shell he ight:ape rture he ight

ratio s in

P.·

antipodum.

9 . "Di c e-grams" showing variation in she l l·

measurement ratio s in s e l e cted populat' ions o f

P.

-antinodum .

14

21

22

.LA

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Fi gure Fo l l o win g page 10. "D:i.c e-gra ms11 sho vving va ria tion in she l l

mea suremen t ra ti o s i n po pulation s o f

P.

puno id e s and

_P.

e stuarin us.

11. "Di c e-gra ms''. sho wi ng varia tion in she l l mea suremen t ra tio s o f P. anti podum from three po pul a tions a t-- 12 mon thly in te rva l s.

12. Co mpa ra ti ve gra phic a l re pre sentation o f va ria tion in she l l sha pe in the three spec i e s o f Po ta mopyrgus.

13. Outl ine tra c ings o f she l l s sho win g ran ge o f va ria tio n in sha pe and o rnamentati on in . fi ve po pulation s o f P. anti pod um.

l L�. Ra dula , ·o pe rcul um, e _m?ryo ' she l l s, an i ma l e xtende d, and he ad pi gmenta tion o f

Fo ta mo uyrgus spp.

15.

16.

17.

18.

19.

(a ) Numbe rs o f serra tio n s on marg � a l te e th in ,thre e popula tions o f P. a nti nodum.

(b ) Number o f ro ws o f te eth per un it length of rad ul a in Po ta mo nyrgus spp.

Rad ula l en gth pl o tte d a ga i nst shel l he i ght in Po ta mo nyrgus spp.

Mal e reprod uc ti ve syste m.

Fema l e reprod uc tive system.

Ul tra -vio l et fl uo rescen c e and abso rption pa tt e rn s o bta ined fro m fo o t_rnusc l e squa she s o f fo ur spe c i e s o f·Gastro poda . .

22

23

24

30

32

32 38 41

54

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!igure Follo·wing page

20.

Free amino acid patterns obtained on chromatographing foot muscle and mantle edge tissue of four species of Gastropoda.

21.

Relationships between shell height, shell form, shell encrustment, and type of

habitat, in

P.

antipodum.

22.

Distribution of Potamon;{rgus spp. in an arm of Hobson Bay, Auckland, in relation to water salinity.

23.

Selection of. submerged and exposed sub- strata by P. estuarinus and

P.

antipodum in laboratory experiments.

24.

:3urvi val time of Potamopyrgus spp. at · .

lOO

%

PJI on a damp substr.ate at

20-26°C.

25.

Suggested steps irr the evolution. of the New Zealand species of Potamopyrgus.

26. (a) Air temperatures recorded at Grasslands Division, D;S.I.R., Palmerston North;

March

1965 -

_April

1966 ..

(b)

Diurnal air ·and water temperatures recorded

in

Tiritea�Stream valley,

September

199.9.

27.

Monthly 'Size structures of· three pop:ulp.tions

2,..,

_o.

of P ^{• .}a.ntinodum from April

1965-April 1966.

Population structure in Pqnd A. dt1,ririg .the ..

55

65

69

73

78

92

103

111

period between draining and refilling,

1965. 112

xi

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:D'o ^llowi nr:r nage

29.

Numbers of er.1bryos present each month in gravid

femal�i

f�om three populations of

P. antinodum.

. .

30.

hlean growth of four laboratory populations of P. antinodum.

31.

Diagram of a section of Tiri�ea Stream

shmYinr; position of drift net� ·

32. 3xperimental a.pparatu's used to produce superoxye;enated conditions' a.t ·above

. .

ambient temperathres.

33.

l:,fumbel·s of snails active at experimental temperatures between ²⁶ ajld

30°C.

34.

The trematode parasites of P. antinodum recorded.by'hlacfarlane.

35.

Trematode parasites of Fotamoriyrgus �pp.;

·

_Monostome cercariae.

36.

Trematode parasites of

P. a

n

tin o

_d

um�

11?

121

130

137

138 141

1LJ-1

:B'urcocercariae, Cercar·iaea,

X

iphidiocercariae.

147 37.

Trematode parasites of F. antinod.um;

Gymnocephalu-s cercariae.

38 .

The protozoan (Sporozoa :· Porospo�id

�

^e

Y

parasite of P. antioodum;

sporozoite.

·

39.

The protozoan parasite of P. anti

:O

^odum.;

·

cysts.

LJ-0. The oligochaete Chaetogaster limnaei limnaei -vvi th

shells of embryonic

_P. antinodum visible

151

157

15'7

in the gut.

159

:x:ii