NIOZ-RAPPORT 1 9 9 9 - 7
9
4
SPECIES-ENVIRONMENT RELATIONSHIP IN MARINE
SOFT-BOTTOM COMMUNITIES: REGRESSION
MODELING AND THE IMPLICATIONS OF SCALE
J. van der Meer & P.J.C. Honkoop
Nederlands Instituut voor Onderzoek der Zee
This report is not to be cited without the
acknowledgement of the source:
Netherlands Institute for Sea Research (NIOZ)
P.O. Box 59, 1790 AB Den Burg, Texel
The Netherlands
ISSN 0923 - 3210
Cover design: H. Hobbelink
V H Z (vzw)
VLAAMS INSTITUUT VOOR DE Z E f
(■L A N D E R S M A R IN E IN S T IT U T E
O o s te n d o - B elgium
SPECIES-ENVIRONMENT RELATIONSHIP IN MARINE
SOFT-BOTTOM COMMUNITIES: REGRESSION
MODELING AND THE IMPLICATIONS OF SCALE
Jaap van der Meer & Pieter J.C. Honkoop
This report presents the results of a study commissioned by the
National Institute for Coastal and Marine Management / RIKZ (Rijkswaterstaat)
NETHERLANDS INSTITUTE FOR SEA RESEARCH (NIOZ)
NIOZ-RAPPORT 1999-7
ABSTRACT
A lite ra tu re stu d y w as p e rfo rm e d a im in g to e x p lo re th e re la tio n b e tw e e n th e sp a tia l sc a le o f m a rin e
b e n th ic su rv e y s an d th e o b s e rv e d g o o d n e s s-o f-fit o f re g re s sio n m o d e ls re la tin g a n im a l a b u n d a n c e to
th e e n v iro n m e n t. A fu rth e r o b je c tiv e w as to ta b u la te th e a b io tic fa c to rs an d p ro c e s s e s th a t p re d o m i­
n a n tly e x p la in th e v a ria tio n in a b u n d a n c e an d to e x a m in e w h e th e r o r n o t th e ty p e o f im p o rta n t fa c ­
to rs d iffe r in re la tio n to th e sc a le o f th e study. S in g le stu d ie s in w h ic h b e n th o s -e n v iro n m e n t re g re s ­
sio n m o d e ls w e re a p p lie d at d iffe re n t sp a tia l sc ale s an d w h ic h w o u ld h a v e a llo w e d a w ith in -stu d y
c o m p a riso n o f th e g o o d n e s s -o f-fit in re la tio n to scale, w ere n o t fo u n d . T h e p a u c ity o f stu d ie s th at
re p o rte d q u a n tita tiv e in fo rm a tio n and, if th e y d id so, th e u se o f a v a rie ty o f in c o m p a ra b le sta tistic a l
m o d e ls re su lte d in v e ry fe w o b se rv a tio n s an d a la ck o f sta tistic a l p o w e r o f th e (b e tw e e n -s tu d y ) re ­
la tio n b e tw e e n sc a le an d g o o d n e s s-o f-fit. M o st stu d ie s c o n firm e d th e im p o rta n c e o f s e d im e n t c h a r ­
a c te ris tic s an d e le v a tio n (in c a se o f in te rtid a l areas) o r w a te r d e p th (in c a s e o f su b tid a l a re as) in d e ­
te rm in in g th e b en th o s. F u rth e r stu d ie s on th e im p o rta n c e o f th e sp a tia l sc ale o f m a rin e b e n th o s-e n v iro n m e n t su rv e y s sh o u ld b e b a s e d on a u n ifie d an a ly tic a l a p p ro a c h , w h ic h ca n o n ly b e re a liz e d if
o rig in a l d a ta are a v a ila b le .
IN T R O D U C T IO N
Objectives
R ijk sw a te rsta a t, w h ic h is p a rt o f th e D u tc h M in istry o f T ra n sp o rt a n d P u b lic W o rk s , is c o -re s p o n sib le fo r th e m a n a g e m e n t o f co a sta l a n d e s tu a rin e e c o sy s te m s in th e N e th e rla n d s. T h e b e n th ic so ftse d im e n t fa u n a fo rm s an e ssen tial e le m e n t o f th e se e c o sy ste m s. H u m a n im p a c t o n th is fa u n a , fo r
e x a m p le b y m e a n s o f in fra -stru c tu ra l w o rk s, m in in g , an d d re d g in g , o fte n w o rk s th ro u g h c h a n g e s in
th e a b io tic e n v iro n m e n t. K n o w le d g e o f th e re la tio n sh ip s b e tw e e n th e a b io tic e n v iro n m e n t a n d th e
b e n th ic fa u n a is th e re fo re fu n d a m e n ta l fo r a re lia b le im p a c t a sse ssm e n t. T h e m o s t c o m m o n ly a p ­
p lie d re se a rc h m e th o d to e s tim a te su ch re la tio n sh ip s is to p e rfo rm a sp a tia l su rv e y , in w h ic h d a ta on
sp e c ie s a b u n d a n c e an d e n v iro n m e n ta l c o n d itio n s are g a th e re d at a la rg e n u m b e r o f s a m p lin g sites.
S u b se q u e n tly reg re ssio n m o d e ls are fitte d , in w h ich sp e c ie s a b u n d a n c e is s u p p o se d to d e p e n d o n th e
e n v iro n m e n t. T w o e x a m p le s w ith in th e D u tch c o n te x t o f th e u se o f k n o w n re la tio n sh ip s b e tw e e n
th e a b io tic e n v iro n m e n t an d th e b e n th ic f a u n a fo r im p a c t a s s e ss m e n t are (1) th e a-posteriori
e v a lu a tio n o f th e im p a c t o f th e co n s tru c tio n o f th e sto rm -su rg e b a rrie r in th e O o ste rs c h e ld e o n th e
a b u n d a n c e o f th e in te rtid al b en th o s, e v a lu a te d at th e sp e cie s le v e l (V an d e r M e e r 1999), a n d (2) th e
a s s e ss m e n t o f th e im p a c t o f su b sid e n c e as a re su lt o f g as w in n in g on th e to tal m a c ro z o o b e n th ic
b io m a ss (B e u k e m a 1998a, B e u k e m a 1998b). In b o th c a se s th e im p a c t w o rk e d th ro u g h c h a n g e s in
th e e le v a tio n o f th e in te rtid al area.
A im o f th e p re se n t stu d y is to e v a lu a te th e sc ie n tific lite ra tu re in w h ic h su c h sp e c ie se n v iro n m e n t m o d e ls fo r th e b e n th ic fa u n a o f so ft-se d im e n t co a sta l an d e s tu a rin e e c o sy s te m s are
u sed. S p ecial e m p h a sis w ill b e p la c e d on sc ale asp ec ts, b e c a u s e th e ty p e o f a b io tic v a ria b le s th a t
a p p e a r to b e im p o rta n t and th e e x p la n a to ry stren g th o f th e m o d e ls m a y h e a v ily d e p e n d o n th e sc ale
o f th e stu d y . In sh o rt, w e w ill:
• p ro v id e an o v e rv ie w o f sc ie n tific stu d ies in w h ic h s p e c ie s-e n v iro n m e n t re la tio n sh ip s h a v e b ee n
q u a n tifie d , b u t re stric te d to th e b e n th ic fa u n a o f c o a sta l an d e s tu a rin e so ft-se d im e n t e c o sy ste m s;
• re la te th e fra c tio n o f th e o v era ll v aria tio n in th e a b u n d a n c e o f b e n th ic sp e c ie s th a t is e x p la in e d b y
th e a b io tic e n v iro n m e n t to th e sp a tia l sc ale (w h ich m a y ra n g e fro m th e sc a le o f a re g io n , fo r e x a m ­
p le in c lu d in g th e D u tc h W a d d e n S e a an d th e D u tc h D e lta , to th e sc ale o f an e s tu a ry , e.g . th e
W e ste rs c h e ld e , an d fu rth e r d o w n to th a t o f a sin g le m u d fla t).
• ta b u la te th e a b io tic fa c to rs an d p ro c e sse s th a t p re d o m in a n tly e x p la in th e v a ria tio n in a b u n d a n c e
a n d e x a m in e w h e th e r o r n o t th e ty p e o f im p o rta n t fa c to rs d iffe r in re la tio n to th e sc ale o f th e stu d y .
N e w a n a ly se s u sin g o rig in a l d a ta are b e y o n d th e sc o p e o f th e p re se n t study.
Scale
O rg a n ism s are n o t h o m o g e n e o u s ly d istrib u te d in sp ace. E c o lo g ists aim to u n d e rs ta n d th e se h e te ro ­
g e n e o u s sp a tia l p a tte rn s in te rm s o f th e p ro c e sse s th a t p ro d u c e th e m (L e v in 1992). B o th p h y sic a l
fa c to rs an d b io lo g ic a l p ro c e sse s m a y g e n e ra te an d m a in ta in sp a tia l v a ria tio n in p o p u la tio n d e n sitie s.
T h e re la tiv e ro le o f p a rtic u la r p h y sic a l fea tu re s a n d p ro c e sse s in g o v e rn in g th e sp a tia l p a tte rn
o f sp e c ie s a b u n d a n c e w ill d e p e n d on th e sc a le th a t is u se d (B a rry a n d D a y to n 1991). D iffe re n c e s in
sp e cie s c o m p o s itio n on a w o rld w id e sc ale , e.g. b e tw e e n p o la r an d tro p ic a l re g io n s, c a n b e e x p la in e d
b y th e u n e v e n h e a tin g o f th e su rfa c e o f th e ea rth a n d th e re su ltin g te m p e ra tu re d iffe re n c e s. O n th e
o th e r h an d , it is m o st u n lik e ly th a t te m p e ra tu re d iffe re n c e s are re le v a n t on a m ic ro -s c a le o f a few
s q u a re d c e n tim e te rs o f o c e a n b o tto m . T h e im p o rta n c e o f p a rtic u la r b io lo g ic a l p ro c e s s e s is also
sc a le -d e p e n d e n t (S c h n e id e r 1994, M c A rd le et al. 1997, S c h n e id e r e t al. 1997). M a th e m a tic a l
m o d e ls, e.g. re a c tio n -d iffu sio n m o d e ls an d c e llu la r a u to m a ta m o d e ls, su g g e st th a t sp a tia l v a ria tio n
in p o p u la tio n d e n s ity on a local sc ale ca n b e th e re su lt o f b io lo g ic a l p ro c e ss e s su ch as lim ite d
d isp e rs a l o f p ro p a g u le s (O k u b o 1980, M u rra y 1989, P h ip p s 1992). H e te ro g e n e ity o n a sp a tia l sc ale
la rg e r th a n th e m o b ility o f an in d iv id u a l m a y b e th e re su lt o f p e rio d ic o r c h a o tic d y n a m ic s w h ich
are n o t s y n c h ro n iz e d a c ro ss d iffe re n t are as (H a sse ll et al. 1991).
T h e p ro b le m o f u n d e rs ta n d in g sp a tia l p a tte rn s in an im al a b u n d a n c e is as c o m p le x as e c o lo g y
its e lf a n d an o v e rw h e lm in g v a rie ty o f re se a rc h m e th o d s h as b ee n a p p lie d to c o n trib u te to a fu rth e r
co m p re h e n sio n . In th e p re s e n t p a p e r w e th e re fo re fo c u s on a sp e c ific re s e a rc h a p p ro a c h , th a t is, as
w as sa id e a rlie r, re g re ssio n m o d e lin g on th e b asis o f su rv e y d ata. M o re s p e c ific a lly , w e fo c u s on the
w id e ly a p p lie d re se a rc h m e th o d w h e re (1) o n e o r m o re o b se rv a tio n a l fie ld su rv e y s in w h ic h d a ta on
sp e c ie s a b u n d a n c e an d e n v iro n m e n ta l c o n d itio n s are g a th e re d at a la rg e n u m b e r o f sa m p lin g sites,
are p e rfo rm e d ; an d w h e re (2 ) a re g re ssio n m o d el is fo rm u la te d u n d e r th e a s su m p tio n th a t sp e cie s
a b u n d a n c e d e p e n d s on th e (sp a tia l) e n v iro n m e n t. W e also re stric t o u rse lv e s to stu d ie s o f c o a sta l an d
e s tu a rin e s o ft-b o tto m c o m m u n itie s.
A s w a s sa id e a rlie r, aim o f th e p re se n t stu d y is to e x p lo re to w h a t e x te n t th e o b se rv e d sp e c ie se n v iro n m e n t re la tio n s h ip s are sc a le -d e p e n d e n t. D o es a re la tio n e x is t b e tw e e n th e sp a tia l sc a le o f th e
stu d y an d th e e s tim a te d re g re ssio n m o d e l? W e rev ie w th e e x istin g lite ra tu re on sp e c ie s -e n v iro n m e n t
re la tio n sh ip s in c o a sta l an d e s tu a rin e so ft-b o tto m c o m m u n itie s. W e e x a m in e w h e th e r a re la tio n sh ip
e x is ts b e tw e e n th e s c a le o f a stu d y an d th e e x p la n a to ry stre n g th o f th e re g re ssio n m o d e l th a t h as
b een u se d . W e also lo o k at th e a b io tic fa c to rs th a t p la y an im p o rta n t ro le an d try to a n s w e r th e
q u e s tio n w h e th e r d iffe re n t so rts o f fa c to rs c o n trib u te in s m a ll-sc a le stu d ie s c o m p a re d to th o se in
la rg e -s c a le stu d ies.
The Gaussian Response Model
In e c o lo g y fittin g re g re ssio n m o d e ls th a t rela te sp e c ie s a b u n d a n c e to e n v iro n m e n ta l v a ria b le s is
k n o w n as d ire c t g ra d ie n t an a ly sis (W h itta k e r 1967). T h e o b je c tiv e o f d ire c t g ra d ie n t a n a ly sis m a y
b e n o te d as to p ro v id in g a p a rsim o n io u s d e sc rip tio n o f th e c o m m u n ity (re stric te d in s p a c e an d tim e
to th e stu d y a re a an d stu d y p e rio d ) in te rm s o f a m u ltiv a ria te re g re ssio n m o d e l th a t re la te s sp e c ie s
a b u n d a n c e to e n v iro n m e n ta l v a ria b le s. T h e te rm m u ltiv a ria te re fe rs to th e fa c t th a t u s u a lly m o re
th a n o n e sp e c ie s is in v o lv e d .
T h e m o st fa v o re d re g re ssio n m o d e l to d e sc rib e th e d e p e n d e n c e o f sp e c ie s o n th e ir e n v iro n ­
m e n t is th e G a u ss ia n re sp o n se m o d e l (G a u ch an d C h a se 1974, G a u c h e t al. 1974). T h e re g re s sio n
m o d e l h as a bell sh a p e, i.e. it h as th e fo rm o f an o p tim u m fu n c tio n an d m o re o v e r ca n o n ly g iv e
p o sitiv e v a lu e s fo r sp e c ie s a b u n d a n c e . T h e n am e G a u s s ia n ste m s fro m th e m a th e m a tic a l sim ila rity
to th e N o rm a l o r G a u ss ia n p ro b a b ility d e n sity fu n c tio n . In its sim p le st fo rm , th a t is fo r a sin g le e n ­
v iro n m e n ta l v a ria b le , the G a u ss ia n re sp o n se m o d e l is g e n e ra lly w ritte n as
y ij = exp
i = ! ,• •• ,« refers to th e site s; j =
, w h ere th e in d e x
'
to th e
2 tj
sp e c ie s; y-,j is th e a b u n d a n c e at site i o f sp e cie s j\ xt is th e v alu e o f th e e n v iro n m e n ta l v a ria b le at site
i\ ex p (cy) is th e m a x im u m a b u n d a n c e o f sp e cie s j; mj is th e o p tim u m fo r sp e c ie s j, th a t is th e v alu e
o f th e e n v iro n m e n ta l v a ria b le w h ere sp e cie s j h as its m a x im u m a b u n d a n c e ; tj is th e to le ra n c e o f
sp e c ie s j, w h ich is a m e a su re o f th e w id th o f th e re sp o n se cu rv e . F o r m o re th a n o n e e n v iro n m e n ta l
v a ria b le , fo r e x a m p le fo r tw o e n v iro n m e n ta l v a ria b le s, it is m o re c o n v e n ie n t to w rite th e m o d e l as
yu
= e x p (b 0/ + btjx u +b2jxfi + b7ijx 2i + bAjx li + b5jx ux 2j). T h e la tte r e q u a tio n a lre a d y p o in ts to o n e
d isa d v a n ta g e o f fittin g th e G a u ss ia n re sp o n se m o d e l, th a t is th e la rg e n u m b e r o f p a ra m e te rs in
w h ich it m a y resu lt. T h e re su lts c a n n o t b e p re se n te d in o n e o r a few g ra p h ic a l d isp la y s, w h ic h h a m ­
p e rs in te rp re ta tio n . A lte rn a tiv e ly , c o n s tra in ts ca n b e s e t on th e p a ra m e te rs su c h th a t th e G a u ss ia n re(u,-mj)
sp o n se m o d e l can be w ritte n as E^y^ ) = e x p
2 '\
, w h e re all sp e c ie s a re su p p o s e d to
Cj
2 1)
re sp o n d to a sin g le c a n o n ic a l v a ria te u, w h ich is a lin e a r c o m b in a tio n o f th e q e n v iro n m e n ta l v ariab les: u{ = an + 2 ^ aix u ■E stim a tio n o f th e p a ra m e te rs o f th is c o n s tra in e d m u ltiv a ria te G a u ss ia n re/=i
sp o n se m o d e l is n o t stra ig h tfo rw a rd . U su a lly , th e re fo re , a p p ro x im a tin g m e th o d s su c h as C a n o n ic a l
C o rre s p o n d e n c e A n a ly s is (C C sp A ) are u sed . T e r B ra a k (1 9 8 6 ) sh o w e d th a t u n d e r c e rta in a s s u m p ­
tio n s th e re su lts o f C a n o n ic a l C o rre sp o n d e n c e A n a ly sis a p p ro x im a te th e m a x im u m lik e lih o o d e s ti­
m a te s (a ssu m in g a P o is s o n -lik e d istrib u tio n o f sp e c ie s a b u n d a n c e ) o f th e c o n s tra in e d m u ltiv a ria te
G a u ss ia n re s p o n s e m o d e l. C a n o n ic a l C o rre sp o n d e n c e A n a ly s is is n o w p ro b a b ly th e m o s t w id ely
u se d m u ltiv a ria te d ire c t g ra d ie n t an a ly sis m e th o d in c o m m u n ity e c o lo g y (P a lm e r 1993).
W h e n th e e n v iro n m e n ta l g ra d ie n ts are sh o rt c o m p a re d to sp e c ie s to le ra n c e s th e u se o f a lin e ­
a riz e d fo rm o f th e m u ltiv a ria te G a u ss ia n re sp o n s e m o d e l, lik e th e m u ltiv a ria te lin e a r reg re ssio n
m o d e l u sin g lo g tra n s fo rm e d sp e c ie s d e n sitie s, m ay b e m o re a p p ro p ria te (T e r B ra a k a n d P re n tic e
1988, T e r B ra a k 1994). C o n s tra in e d fo rm s o f th e m u ltiv a ria te lin e a r re g re ss io n m o d e l c a n b e re la te d
to th e d im e n s io n a lity -re d u c tio n te c h n iq u e s o f C a n o n ic a l C o rre la tio n A n a ly s is (C C ltA ) an d R e d u n ­
d a n c y A n a ly s is (R A ) (T so 1981, D a v ie s an d T so 1982, J o n g m a n et al. 1987, V a n d e r M e e r 1991).
Implicit regression models, indirect gradient analysis and other multivariate techniques
In so m e c a se s th e sa m e m a th e m a tic a l p ro c e d u re ca n b o th b e in te rp re te d in te rm s o f an o rd in a tio n
te c h n iq u e , p ro v id in g a lo w -d im e n sio n a l re p re se n ta tio n o f th e m u lti-d im e n s io n a l sp e c ie s sp a c e
(w h e re o rig in a lly ea c h d im e n sio n re p re se n ts a sin g le sp e c ie s) o r in te rm s o f a re g re s sio n m o d e l
(L e g e n d re et al. 1997). F o r e x a m p le , C a n o n ic a l C o rre sp o n d e n c e A n a ly s is ca n b e, as w a s sh o w n
ab o v e , in te rp re te d as a re stric te d o rd in a tio n te c h n iq u e o r as an a p p ro x im a tio n to m a x im u m lik e li­
h o o d fittin g (a s su m in g P o isso n erro r) o f a re stric te d G a u ss ia n m o d e l (T e r B ra a k 1985, T e r B raa k
1986). S im ila rly , R e d u n d a n c y A n a ly s is an d C a n o n ic a l C o rre la tio n A n a ly s is c a n b e re g a rd e d as re ­
d u c e d -ra n k lin e a r re g re ssio n m o d e ls (Jo n g m a n et al. 1987, V an d e r M e e r 1991). In so m e stu d ie s the
o rd in a tio n in te rp re ta tio n has b ee n p re se n te d . W e h av e , h o w e v e r, a lw a y s in te rp re te d th e re s u lts, as
fa r as p o ssib le , in te rm s o f re g re ssio n m o d e ls.
In d ire c t g ra d ie n t a n a ly sis is th e ec o lo g ic a l e q u iv a le n c e o f (la te n t) fa c to r a n a ly sis. T h e
te c h n iq u e o f f a c to r a n a ly sis e s tim a te s fo r ea c h site th e v a lu e s o f o n e o r m o re so -c a lle d la te n t fa c to rs,
u n d e r the a s su m p tio n o f so m e sp e c ifie d ty p e o f re la tio n s h ip b e tw e e n th e la te n t fa c to r(s ) an d th e
sp e cie s a b u n d a n c e d ata. T h e s e la te n t fa c to r v a lu e s a re e x p e c te d to re p re se n t e n v iro n m e n ta l g ra d i­
en ts. E x a m p le s o f fa c to r a n a ly tic a l te c h n iq u e s are P rin c ip a l C o m p o n e n t A n a ly s is (P C A ) a n d C o rre ­
s p o n d e n c e A n a ly s is (C A ). P rin c ip a l C o m p o n e n t A n a ly s is is b a s e d u p o n th e a s s u m p tio n o f a lin e a r
re la tio n s h ip
b e tw e e n
sp e c ie s
abundance
an d
e n v iro n m e n ta l
g ra d ie n ts
(la te n t
fa c to rs).
C o rre s p o n d e n c e A n a ly s is b u ild s on th e a ssu m p tio n o f a u n im o d a l re la tio n s h ip b e tw e e n sp e cie s
a b u n d a n c e a n d e n v iro n m e n ta l g rad ie n ts.
M a n y o th e r m u ltiv a ria te te c h n iq u e s c a n n o t e a sily b e in te rp re te d in te rm s o f a re g re s sio n
m o d e l. O n e o f th e a p p ro a c h e s w h ic h h as re c e n tly b ee n p u t on th e fo re g ro u n d is b a s e d on th e (h a r­
m o n ic
ran k )
c o rre la tio n
b etw e en
th e
sp e c ie s
(d is)sim ila rity
m a trix
and
th e
e n v iro n m e n t
(d is)sim ila rity m a trix (C la rk e an d A in sw o rth 1993). A d d itio n a lly , th e a p p ro a c h u se s n o n -m e tric
M u ltiD im e n sio n a l S c a lin g (M D S ) o f th e tw o (d is)s im m ila rity m a tric e s to v isu a liz e se th e re la tio n ­
s h ip b e tw e e n sp e c ie s a n d e n v iro n m e n ta l v aria b les.
Goodness-of-fit
T h e p re se n t stu d y fo c u se s on th e g o o d n e s s-o f-fit o f m u ltiv a ria te re g re ssio n m o d e ls, w h ic h aim to
re la te sp e c ie s a b u n d a n c e to th e e n v iro n m e n t. G en e ra lly , th e g o o d n e s s-o f-fit te rm q u a n tifie s th e e x ­
p la n a to ry p o w e r o f th e re g re ssio n m o d e l, b u t th e ac tu al g o o d n e s s -o f-fit m e a s u re is n e c e s sa rily
stro n g ly lin k e d to th e a s su m e d e rro r stru c tu re o f th e m o d e l. F o r e x a m p le , fo r le a st-sq u a re s m o d e ls
(w h ich a re e q u iv a le n t to the m a x im u m lik e lih o o d m e th o d if th e e rro rs a re N o rm a lly d is trib u te d ) th e
u su a l g o o d n e s s -o f -fit m e a su re is R2, th e fra ctio n e x p la in e d v aria n ce . T h is fra c tio n is g iv e n b y o n e
m in u s th e ratio o f th e resid u a l su m o f sq u a re s to th e to ta l su m o f sq u a re s. F o r o th e r a s su m p tio n s
a b o u t th e e rro r d istrib u tio n , a lte rn a tiv e g o o d n e s s-o f-fit m e a s u re s h a v e to be u se d . T h e c la ss o f g e n ­
e ra liz e d lin e a r m o d e ls u se s th e d e v ia n c e as a g e n e ra liz a tio n o f th e su m -o f-sq u a re s a n d g o o d n e s s -o ffit is e x p re sse d as p e rc e n ta g e e x p la in e d d ev ian c e.
Classification
In sh o rt, stu d ie s w ere c a te g o riz e d as fo llo w s:
1) u n iv a ria te m o d e ls, d e p e n d e n t v a ria b le is sp e cie s a b u n d a n c e ;
2) u n iv a ria te m o d e ls, d e p e n d e n t v a ria b le is a c o m m u n ity a ttrib u te (e.g . so m e d iv e rs ity m e a su re ,
to tal a b u n d a n c e , etc.);
3)
lin e a r d ire c t g ra d ie n t a n a ly sis, i.e. C c ltA o r R A ;
4)
n o n -lin e a r d ire c t g ra d ie n t a n a ly sis, i.e. C C sp A ;
5)
lin e a r in d ire c t g ra d ie n t an a ly sis, i.e. a m u ltiv a ria te la te n t fa c to r m o d e l (P C A ) c o m b in e d w ith
u n iv a ria te m o d e ls to re la te th e la ten t fa c to rs to o b se rv e d e n v iro n m e n ta l v a ria b le s;
6) n o n -lin e a r in d ire c t g ra d ie n t a n a ly sis, i.e. a m u ltiv a ria te la te n t fa c to r m o d e l (C A ) c o m b in e d w ith
u n iv a ria te m o d e ls to re la te th e la ten t fa c to rs to o b se rv e d e n v iro n m e n ta l v a ria b le s;
7 ) h a rm o n ic ran k c o rre la tio n b e tw e e n th e sp e cie s (d is)s im ila rity m a trix an d th e e n v iro n m e n t
(d is)sim ila rity m a trix , in c o m b in a tio n w ith M D S .
The scale o f macrobenthos surveys
U su a lly , n o t m u c h a tte n tio n is p aid to in te rp re tin g the resu lts o f a b e n th o s s u rv e y (i.e. th e e x p la n a ­
to ry stre n g th o f th e re g re ssio n m o d e l an d th e ty p e o f e n v iro n m e n ta l v a ria b le s th a t a p p e a re d to be
im p o rta n t) in te rm s o f th e sc a le o f th e stu d y . W e are n o t a w a re o f a n y stu d y in w h ic h b e n th o s-e n v iro n m e n t re g re ssio n m o d e ls are a p p lie d at d iffe re n t sp a tia l sc ale s w ith in a sin g le a re a , a llo w in g a
c o m p a riso n o f the g o o d n e s s-o f-fit. O n e n o tic e a b le ex c e p tio n (a lth o u g h q u a lita tiv e ) is F la c h (1 9 9 6 ),
w h o o b se rv e d th a t th e la rg e r sc a le p a tte rn s in th e d istrib u tio n o f Corophium in th e W a d d e n S e a are
d e te rm in e d by p h y sic a l fa c to rs , su ch as se d im e n t c o m p o sitio n an d e le v a tio n . T h e s m a lle r sc a le p a t­
te rn s are re la te d to b io lo g ic a l in te ra c tio n s, i.e. c lu ste rs o f ju v e n ile s aro u n d b u rro w s o f a d u lt fe m a le s.
T h e sc a le o f a sa m p lin g su rv e y c o n s ists o f tw o p a rts, th e u n it an d th e fra m e (C o c h ra n 1977).
T h e u n it is th e sm a lle s t ite m th a t is sa m p le d in th e su rv ey . In b e n th o s s u rv e y s it is th e a re a o f th e
sa m p lin g d e v ic e . T h e fra m e is th e list o f all p o ssib le u n its. S ta te d o th e rw ise , th e to ta l s tu d y a re a (th e
fra m e ) can be th o u g h t o f as c o m p risin g a fin ite n u m b e r (an d u su a lly la rg e ) o f sm a ll n o n -o v e rla p p in g are as (th e u n its ), e a c h o f th e siz e o f th e sa m p lin g d ev ice . In ste a d o f u s in g th e s ta tistic a l te rm s
fra m e a n d u n it, o th e r te rm s are in u se as w ell, e x te n t an d g rain (W ie n s 1989), fie ld o f v ie w an d
g rain (V an d e r M e e r 1997), m a x im u m o u te r scale an d m in im u m in n e r sc ale, o r ra n g e a n d re so lu tio n
(S c h n e id e r 1994).
M A T E R IA L A N D M E T H O D S
A c o m p u te riz e d lite ra tu re s u rv e y w a s p e rfo rm e d u sin g Online Contents, a d a ta b a s e c o n ta in in g the
c o n te n ts o f 12,500 sc ie n tific an d n o n -sc ie n tific jo u rn a ls an d m a g a z in e s. It is p o s s ib le to se a rc h fo r
lite ra tu re p u b lis h e d sin c e S e p te m b e r 1992. W e se a rc h e d fo r th e fo llo w in g k e y w o rd s (o r c o m b in a ­
tio n s of): (m a rin e ) (m a c ro ) b e n th o s, m a c ro fa u n a , m u ltiv a ria te (a n a ly se s), in te rtid a l (as in itia lly w e
w a n te d to re stric t o u r a n a ly sis to in te rtid al are as), sc ale p a tte rn , b e n th o s o r b e n th ic su rv e y , d is trib u ­
tio n p a tte rn (s) a n d sp a tia l sc ale . T h is lite ra tu re s u rv e y y ie ld e d 37 titles, b u t o n ly tw o p a p e rs co u ld
be u sed . O n ly th e se p a p e rs (ref. 5 an d ref. 14) re p o rte d a q u a n tita tiv e a n a ly sis o f th e re la tio n b e ­
tw ee n th e b e n th ic c o m m u n ity o f an in te rtid al a re a an d a b io tic facto rs.
In re c e n t p u b lis h e d , p o ssib ly n o t y et c o m p u te riz e d , lite ra tu re w e fo u n d o n e s u ita b le p a p e r (ref.
14). A stu d y o f 4 8 in te rn al re p o rts, m a in ly c o n c e rn in g m a rin e b e n th o s o f D u tc h c o a sta l s y s te m s an d
e s tu a rie s an d th e N o rth S ea, re v e a le d 4 stu d ie s fro m w h ich w e c o u ld a b stra c t u se fu l d ata.
A s e c o n d c o m p u te riz e d su rv e y w as p e rfo rm e d u sin g th e DIALOG d a ta se a rc h e n g in e . W e
lo o k e d fo r in th e fo llo w in g a rc h iv e s, Oceanic Abstracts (re fe re n c e s a v a ila b le sin c e 1964) an d
Aquatic Sciences and Fisheries Abstracts (re fe re n c e s a v a ila b le sin c e 1978). T h e fo llo w in g c o m b i­
n a tio n s o f k e y w o rd s w e re u sed: b en th o s o r b e n th ic , c o m b in e d w ith m a rin e an d m u ltiv a ria te an d in ­
te rtid a l o r in te r-tid a l an d m a c ro fa u n a o r m a c ro z o o b e n th o s c o m b in e d w ith in te rtid a l a n d m u ltiv a ri­
ate. T h is s u rv e y y ie ld e d in to tal 6 0 titles. F ro m th e a b stra c ts, w e s e le c te d 2 6 p a p e rs fro m w h ic h at
la st o n ly 14 h ad e n o u g h q u a n tita tiv e d etail to b e su ita b le fo r o u r a n a ly sis (ref. 1-4, 6 -1 2 , 15, an d
16). F ro m th e se 14 re fe re n c e s, tw o are d e a lin g w ith a su b tid al e n v iro n m e n t (ref. 3 a n d 13).
B e c a u se lite ra tu re a b o u t m a rin e in te rtid al b e n th o s an d a b io tic s tru c tu rin g fa c to rs se e m e d to b e
s c a rc e (o n ly 16 re fe re e d p a p e rs an d 4 in te rn al re p o rts) w e d e c id e d to e x te n d o u r su rv e y to su b tid a l
re g io n s. A g ain a c o m p u te riz e d su rv e y in th e Oceanic Abstracts an d Aquatic Sciences and Fisheries
Abstracts a rc h iv e s w as p e rfo rm e d u sin g th e DIALOG d a ta se a rc h e n g in e. T h e a b o v e m e n tio n e d
k e y w o rd s w e re u se d b u t in ste a d o f in te rtid a l, th e k e y w o rd s su b tid a l o r su b -tid a l w e re u se d . T h is
se arch y ie ld e d o n ly 7 titles, fro m w h ic h o n e (ref. 3) w as a lre a d y k n o w n . F ro m th e re m a in in g six
re fe re n c e s, tw o d id n o t p ro v id e th e re q u ire d q u a n tita tiv e in fo rm a tio n .
T h e lists o f lite ra tu re re fe re n c e s w ith in th e se le c te d p a p e rs a n d re p o rts y ie ld e d a fe w m o re ti­
tle s th a t w e re su ita b le fo r fu rth e r stu d y .
F o r e a c h stu d y , g rain (m 2) is d e fin e d as th e s a m p le d su rfa c e a re a p e r sta tio n , an d e x te n t (k m )
as th e m a x im u m d ista n c e b e tw e e n sta tio n s.
RESULTS
Studies and scales
T h e lite ra tu re su rv e y y ie ld e d e v e n tu a lly 32 stu d ies (W a rw ic k 1971, L ie 1978, M o o re 1978, P o o re
an d M o b le y 1980, H o g u e a n d M ille r 1981, W h itla tc h 1981, E ss e lin k an d V an B e lk u m 1986, R a ffaelli et al. 1986, D e G ee an d D e k k e r 1987, P e a rso n an d R o s e n b e rg 1987, G ra y e t al. 1988, Z w a rts
1988, A u ste n an d W a rw ic k 1989, E llio tt an d O 'R e illy 1991, M e ire e t al. 1991, R a ffa e lli e t al. 1991,
V an d e r M e e r 1991, D e fe o et al. 1992, G ee e t al. 1992, B u h l-M o rte n s e n an d H 0 is æ te r 1993,
Ja ra m illo an d M c L a c h la n 1993, S un et al. 1993, Ja ra m illo 1994, H a y n e s an d Q u in n 1 995, S o e ta e rt
et al. 1995, B a c h e le t e t al. 1996, M c la c h la n 1996, L e g e n d re e t al. 1997, N e tto an d L a n a 1997, O u g
1998, O u g e t al. 1998). M a c ro b e n th o s stu d ies w e re m u ch m o re c o m m o n th a n m e io b e n th o s stu d ie s
(T a b le 1). M o st o f th e stu d ie s w e re p e rfo rm e d in in te rtid a l are as in th e te m p e ra te z o n e (T a b le 2).
T h e g rain o f th e m a c ro b e n th o s stu d ie s ran g e d fro m 0 .0 1 5 to 3.3 m 2 (a p a rt fro m o n e o u tlie r, w h e re
th e g rain w as 2 5 0 m 2), an d th e e x te n t fro m 0 .0 2 5 to 4 5 0 k m (T a b le 1, F ig . 1). If o n ly th e
m a c ro b e n th o s stu d ie s are ta k e n in to ac co u n t, th e re la tiv e v a ria b ility in g ra in ( SD(log grain) = 0 .5 7 ,
n = 2 5 ) w a s s m a lle r th a n th e re la tiv e v a ria b ility in e x te n t ( SD(log extent) = 1.08, n = 2 5 ). N o s ig ­
n ific a n t c o rre la tio n ( r = 0 .1 0 , n = 25, P = 0 .6 2 ) b e tw e e n g rain an d e x te n t w a s o b se rv e d (F ig . 1). T h e
re la tiv e ly low v a ria b ility in g ra in is p re su m a b ly th e re su lt o f th e u se o f s ta n d a rd iz e d sa m p lin g
e q u ip m e n t an d p ro c e d u re s.
T able 1. An overview o f the 32 selected studies. G rain in m 2, extent in km , category refers to the type o f analysis (see
text), h abitat (H ab) refers to intertidal (I) or subtidal (S).
1
2
3
4
5
6
7
8
9
10
12
13a
13b
14
15
16
17
18
19
21
22
23
24
25
27
28
29
30
31
101
102
103
2.00E-03
1.90E+00
2.16E-01
4.00E-02
3.10E-07
9.54E-02
9.00E-01
3.30E-01
6.25E-02
3.42E-03
2.50E-01
4.00E-01
4.00E-01
3.30E+00
1.45E-02
5.00E-02
1.00E-01
2.50E-01
4.88E-02
2.88E-03
1.00E-01
2.80E-05
9.00E-01
4.00E-01
4.00E-01
2.50E+02
4.00E-03
6.00E-01
5.00E-02
7.07E-02
4.38E-02
2.00E-01
2000
0.05
18
0.025
.00007
45
50
200
11
12
0.5
450
20
25
30
6
80
0.06
1.5
10
13
0.0012
50
17
15
117
320
10
2
40
4
50
Category
2 4
2
7
6
7
12
6
2
2
5 7
5
7
1
___ 4___
___ 4___
I
Extent
CD
G rain
CM
I
Nr
1_3
6
2
67
2
7
7
2
12
4
67
_2_4___
7
_2 5
__3____
1
1
2
Reference
G roup
Hab
Latitude
Soetaert & Vincx, 1995
Haynes & Quinn, 1995
Bachelet et al., 1996
Netto & Lana, 1997
Sun et al., 1993
Mei re et al., 1991
Jaramillo, 1994
Defeo et al., 1992
Moore, 1978
Austen & Warwick, 1989
Legendre et al., 1997
Oug et al., 1998
Oug et al., 1998
McLachlan, 1996
Van der Meer, 1991
Raffaelli et al., 1986
Elliott & O’Reilly, 1991
Raffaelli et al., 1991
Whitlatch, 1981
Warwick, 1971*
Pearson & Rosenberg, 1987*
Hogue & Miller, 1981
Jaramillo & McLachlan, 1993
Oug, 1998
Gray et al., 1988
Buhl-Mortensen & Hoisæter, 1993
Gee et al., 1992
Lie, 1978
Poore & Mobley, 1980
Zwarts, 1988
Esselink & Van Belkum, 1986
De Gee & Dekker, 1987
Meio
Macro
Macro
Macro
Meio
Macro
Macro
Macro
Macro
Meio
Macro
Macro
Macro
Macro
Macro
Macro
Macro
Macro
Macro
Meio
Macro
Meio
Macro
Macro
Macro
Macro
Meio
Macro
Macro
Macro
Macro
Macro
I
I
479N
38SS
44S40’N
25a33'S
29g15’N
51g50'N
39g35'S
349S
53g30'N
52SN
37g02'S
61gN
61gN
27gS
51S50'N
57Q50'N
56g05'N
57915’N
41g42'N
50°40'N
55g40'N
44g38'N
39g35'S
69g40'N
59g05'N
60g50'N
54g06'N
60g15'N
37S55'S
53g24N
53g18‘N
53g05'N
s
I
I
I
I
I
I
I
I
s
s
I
I
I
s
I
I
I
s
I
I
s
s
s
s
s
s
I
I
s
* See also C larke & W arw ick, 1993.
Various methodologies
G o o d n e s s -o f-fit m e a su re s c a n o n ly be c o m p a re d w ith in ea c h o f th e se v en m e th o d s c a te g o rie s s e p a ­
rately .
R e su lts o f sim p le o r m u ltip le re g re ssio n o f sp e cie s a b u n d a n c e v e rs u s e n v iro n m e n ta l v a ria b le s
(c a te g o ry 1) w e re re p o rte d in 5 stu d ies. T h is low n u m b e r o f stu d ie s d o e s n o t p e rm it a n y c o n c lu ­
sio n s, a lth o u g h th e a v a ila b le d a ta in d ic a te a n e g a tiv e re la tio n s h ip b e tw e e n e x te n t a n d m a x im u m e x ­
p la in e d v a ria n c e (M a x R2). S e e T a b le 3. T h e la ck o f d a ta also h o ld s fo r th e re la tio n s h ip b e tw e e n
c o m m u n ity a ttrib u te s an d en v iro n m e n ta l v a ria b le s (c a te g o ry 2 ), w h ich w e re re p o rte d in 13 stu d ies.
S p e c ie s ric h n e ss, w h ic h w as th e m o st fre q u e n tly re p o rte d c o m m u n ity attrib u te (i.e. in 7 s tu d ie s ), d id
n o t sh o w an y re la tio n w ith sc ale (T a b le 4).
T ab le 2. L atitude and habitat o f the 32 selected studies. M eiobenthos studies betw een brackets. A m sterdam , H olland is
located at 53° N, L isbon, Portugal at about 40° N, and D urban, S outh-A frica or Perth, A ustralia at about 30° S.
Intertidal
Subtidal
Total
> 409 N
309 S to 409 N
< 309 S
8 (4 )
2 (1 )
5
10(1)
0
1
18(5)
2(1 )
6
Total
15(5)
11 (1)
26 (6)
extent (km)
Fig. 1. R elation betw een extent (km ) and grain (m 2) o f a benthos study. Filled dots refer to m acrobenthos studies, open
dots to m eiobenthos studies.
T ab le 3. M axim um R o f five studies in w hich species abundance w as related to environm ental variables. T ype refers to
m ultiple (M ) or sim ple (S) linear regression.
Nr
Grain
12
0.25
102
15
101
24
Extent
Type
0.5
M
0.0438
4
0.0145
30
S
M
0.07068
40
M
0.9
50
S
Independent variables
Shell hash, elevation, shear stress, energy dissipation, water
coverage, wave stirring
Silt, altitude
M ax R2
0.69
0.70
Median grain, altitude and other environmental variables
0.48
Silt, altitude
Mean grain size, beach slope, Dean's parameter
0.39
0.43
T able 4. M axim um R 2 o f seven studies in w hich species richness w as related to environm ental variables. T ype refers to
m ultiple (M ) or sim ple (S) linear regression.
Nr
Grain
Extent
Type
Independent variables
Max FP
Total particle diversity, food particle diversity, % organic matter
Median grain
0.34
0.12
0.85
0.83
19
0.0488
1.5
S
30
14
0.6
10
S
3.3
0.9
25
50
S
Beach slope, sand particle size, sand sorting
Median grain, 1/beach slope, Dean's parameter
Mean grain size, beach slope, Dean's parameter
7
24
103
17
0.9
50
0.2
50
S
S
M
0.1
80
M
Median grain size, silt content, sediment sorting, depth,
distance to shore, distance to MLWL
Water depth, median particle diameter (MPD).silt and clay
content (%SC), sediment sorting (SC), salinity, area
0.91
0.02
0.42
D irec t g ra d ie n t a n a ly sis (c a te g o rie s 3 an d 4 ) w as a p p lie d in six stu d ies. T w o s tu d ie s u se d a lin e a r
te c h n iq u e , i.e. C a n o n ic a l C o rre la tio n A n a ly sis, an d fo u r stu d ie s a n o n -lin e a r m e th o d , C a n o n ic a l
C o rre s p o n d e n c e A n a ly s is. O n e o f th e la tte r stu d ies (n r. 1) d id n o t re p o rt a n y g o o d n e s s -o f-fit
m e a su re , an d th e re m a in in g th ree stu d ies d o not allo w an y su g g e s tio n s fo r p o ssib le re la tio n sh ip s
(T a b le 5).
T able 5. E xtracted variance by the first canonical variate (E V 1), a goodness-of-fit m easure, o f three studies w hich used
C anonical C orrespondence A nalysis to relate species abundance to environm ental variables.
Nr
25
13b
28
13a
Grain
Extent
Type
0.4
0.4
17
20
S
S
250
0.4
117
450
S
S
Independent variables
water depth, TOC, gravel, sorting, fine sand
C/N ratio, water depth, polycyclic aromatic hydrocarbons,
effluent impacted sediment
sill depth, C/N, %Carbon, %Clay
water depth, distance from river, polycyclic aromatic
hydrocarbons, distance from pollution source, effluent
impacted sediment, sand-mixed sediment
EV 1
0.21
0.20
0.35
0.08
In d ire c t g ra d ie n t a n a ly sis (c a te g o rie s 5 an d 6) w a s a p p lie d in n in e stu d ies. T h re e stu d ie s u se d a lin ­
e a r te c h n iq u e , i.e. P rin c ip a l C o m p o n e n t A n a ly s is, an d six stu d ie s a n o n -lin e a r m e th o d , C o rre s p o n ­
d e n c e A n a ly sis. O n ly tw o o f th e la tte r stu d ie s re p o rte d a c o rre la tio n c o e ffic ie n t b e tw e e n o n e o f th e
c a n o n ic a l a x e s an d o n e o r m o re en v iro n m e n ta l v a ria b le s. C le a rly , th is d o e s n o t p e rm it an y s u g g e s ­
tio n s fo r p o s s ib le re la tio n sh ip s.
T h e h a rm o n ic ran k c o rre la tio n b etw e en th e sp e cie s (d is )sim ila rity m a trix an d th e e n v iro n m e n t
(d is )s im ila rity m a trix (c a te g o ry 7 ) w as re p o rte d in fo u r stu d ies. A g a in , th e n u m b e r o f s tu d ie s is n o t
su ffic ie n t fo r an y c o n c lu sio n s (T a b le 6).
T able 6. H arm onic rank correlation betw een the species (dis)sim ilarity m atrix and the environm ent (dis)sim ilarity
m atrix in four selected studies.
Nr
Grain
Independent variables
Extent
r
Spartina biomass, tines, water content, organic content
0.80
10
H2S, salinity, median particle diameter (MPD)
0.80
13
C, Cd, N content of sediment
silt/clay fraction (SCF),depth
0.79
4
0.04
0.025
21
0.00288
22
0.1
29
0.004
320
0.77
F o r ea c h c a te g o ry s e p a ra te ly , sa m p le siz es w ere u n fo rtu n a te ly to o lo w to allo w c o n c lu s io n s . U sin g a
n o n -p a ra m e tric p ro c e d u re , h o w e v e r, c o m b in e s th e re su lts. W e c a te g o riz e d fo r e a c h a n a ly tic a l
m e th o d b o th th e e x te n t an d th e g o o d n e s s-o f-fit in tw o c la sse s: lo w e r th an th e m e d ia n an d h ig h e r
th an th e m e d ian . If th e n u m b e r o f stu d ie s w ith in a c a te g o ry w as u n e v e n , th e m e d ia n w a s p u t in o n e
o f th e tw o c la sse s b y eq u al c h a n c e . T h e c o m b in e d re su lts ca n b e arra n g e d in a tw o -b y -tw o ta b le,
an d th e final re su lt d id n o t p o in t to an y a s so c ia tio n at all (T a b le 7).
T able 7. T he association betw een extent and goodness-of-fit (for each analytical category all figures are clategorized as
low er o r higher than the m edian).
G oodness-of-fit
G oodness-of-fit
low er than m edian
higher than m edian
Sum
E xtent low er than m edian
3
6
9
E xtent h igher than m edian
4
5
9
Sum
7
11
18
Environmental variables
The type of environmental variables that were related to the benthic fauna did not seem to vary
systematically with scale (Table 8). For the intertidal studies, elevation and a variable characterizing
sediment composition (most often median grain size) were the most often mentioned physical fac­
tors correlating with the benthic fauna. For the subtidal studies, water depth instead of elevation was
mentioned. Two studies (nrs. 13 and 22) also considered pollution-related variables, e.g. polycyclic
aromatic hydrocarbons, distance from pollution source, effluent impacted sediment. Few studies
(mainly those concerned with exposed beaches, i.e. nrs. 7, 8, 14 and 24) mentioned variables di­
rectly related to the morpho-dynamic state of the environment, e.g. variables like shear stress, beach
slope and Dean’s parameter (a combination of breaker height, sinking velocity of sand and wave pe­
riod).
T able 8a. E nvironm ental variables that best correlated w ith the benthic fauna, subdivided in general, sedim ent and
w ater-related variables. Intertidal areas.
Nr
Grain
5 3.1E-07
23 0.000028
4
0.04
2
1.9
18
0.25
12
0.25
Extent
65e-6
.00124
0.025
0.05
0.06
0.5
G eneral
Sedim ent •
W ater
elevation
elevation
water, organic matter
elevation
elevation
elevation, shear stress,
energy dissipation, water
coverage, wave stirring
19
0.0488
1.5
102
16
21
9
10
14
15
101
6
0.0438
0.05
0.00288
0.0625
0.00342
3.3
0.0145
0.07068
0.0954
4
6
10
11
12
25
30
40
45
elevation
elevation
24
0.9
50
7
0.9
50
8
0.33
200
beach slope, Dean's
parameter
beach slope, Dean's
parameter
beach slope, Dean’s
parameter
1
0.002
2000
beach slope
elevation
elevation
inundation time
total particle diversity, food
particle diversity, organic
matter
silt
median grain, silt
median grain, H2S
salinity
silt
salinity
mean grain, sorting
median grain
silt
median grain, silt
chlorinity,02 saturation,
POC, suspended matter,
total P, total N, dissolved
Si, dissolved Cd
mean grain
median grain
mean grain
median grain, silt
salinity
T able 8b. E nvironm ental variables that were taken into account in the selected studies, subdivided in general, sedim ent
and w ater-related variables. Subtidal areas.
Nr
Grain
Extent
General
Sedim ent
W ater
31
0.05
2
water depth
30
22
27
25
0.6
0.1
0.4
0.4
10
13
15
17
water depth
water depth
3
0.216
18
water depth
13b
103
0.4
0.2
20
50
17
0.1
80
28
29
13a
250
0.004
0.4
117
320
450
water depth
water depth, distance to median grain, silt, sorting
shore, distance to MLWL
water depth, area
median grain, silt and clay, salinity
sorting
clay, carbon
water depth
silt/clay fraction
water depth
sand-mixed sediment
distance from river
medium sand, fine sand,
silt, clay, sorting
median grain
gravel, fine sand, sorting,
TOC
median grain, gravel, silt,
organic matter, zostera
debris
ortho-phosphate, ammonia,
carbonate
salinity
D IS C U S S IO N
Lack o f power o f the present study
T h e n u m b e r o f a p p ro p ria te stu d ie s th a t w e w e re ab le to se le c t w as u n fo rtu n a te ly ra th e r sm a ll. T h e
m ain re a so n is th a t v ery o fte n a u th o rs d o n o t rep o rt q u a n tita tiv e in fo rm a tio n o n th e g o o d n e s s -o f-fit
o f th e ir m o d e ls, b u t o n ly p ro v id e the p a ra m e te rs o f th e m o d el o r ju s t v isu a lly d isp la y th e re la tio n ­
sh ip . A tim e ly e x a m p le is th e re c e n t stu d y on th e e ffe c t o f su b s id e n c e as a re su lt o f g as e x p lo ita tio n
in th e W a d d e n S ea. A re la tio n sh ip b e tw e e n e le v a tio n an d to ta l b e n th ic b io m a s s w a s fitte d an d s u b ­
s e q u e n tly u se d to asse ss the im p a c t o f c h a n g e s in th e e le v a tio n o f th e m u d fla ts o n to ta l b io m a s s
(B e u k e m a 1998a, B e u k e m a 1998b). T h e g o o d n e s s-o f-fit o f th e a p p lie d m o d e l w as, h o w e v e r, n o t
m e n tio n e d . S ta y in g w ith in th e D u tc h c o n te x t, th e im p re ss iv e h a n d b o o k on th e e c o lo g y o f th e W a d ­
den S e a sh o w s a w e a lth o f (g ra p h ic a l) in fo rm a tio n on th e re la tio n s h ip b e tw e e n th e a b u n d a n c e o f
m a c ro z o o b e n th ic sp e c ie s an d v a rio u s en v iro n m e n ta l fa c to rs (D a n k e rs an d B e u k e m a 1983). G o o d ­
n e s s-o f-fit fig u re s w e re , h o w e v e r, n o t p rese n ted . A fu rth e r p ro b le m th a t w e e x p e rie n c e d w a s re la te d
to th e v a rie ty o f a p p ro a c h e s th a t w e re a p p lie d in th e se le c te d stu d ie s fo r m o d e lin g th e b e n th o s-e n v iro n m e n t re la tio n sh ip . T h e a c c o m p a n y in g g o o d n e s s -o f-fit m e a su re s o f th is v a rie ty o f m o d e ls c a n n o t
be c o m p a re d . F o r ea c h an a ly tic a l m e th o d o n ly v ery few stu d ies w e re a v a ila b le (w ith a m a x im u m o f
se v en stu d ie s w h ich u se d lin e a r re g re ssio n m o d e ls to re la te sp e c ie s ric h n e ss to e n v iro n m e n ta l v a ri­
ab les). In e v ita b ly th is re su lte d in a la ck o f sta tistic a l p o w er. T h e c o m b in e d p ro c e d u re , a lth o u g h it
m ig h t b e la b e le d as a d -h o c , d id n o t p o in t to an y as so c ia tio n b e tw e e n sc a le an d g o o d n e s s-o f-fit.
N e v e rth e le ss, fu rth e r stu d ie s o n th e im p o rta n c e o f th e sp a tia l sc ale o f m a rin e b e n th o s -e n v iro n m e n t
su rv e y s s h o u ld b e b a s e d o n a u n ifie d an a ly tic a l a p p ro a c h , w h ic h ca n o n ly b e re a liz e d if o rig in a l d a ta
are av a ila b le .
Abiotic variables
A lth o u g h the re la tiv e im p o rta n c e o f v a rio u s a b io tic v a ria b le s in re la tio n to sc a le re m a in e d o b sc u re ,
m o st stu d ie s c o n firm e d th e g e n e ra l im p o rta n c e o f se d im e n t c h a ra c te ristic s a n d e le v a tio n (in in te r­
tid al a re as) o r w a te r d ep th (in su b tid a l a re as) in d e te rm in in g th e b en th o s. S o m e stu d ie s (m a in ly on
e x p o s e d b e a c h e s) p o in te d to th e re le v a n c e o f m o rp h o -d y n a m ic s, b y s h o w in g th e e ffe c t o f v a ria b le s
lik e sh e a r stre ss a n d D e a n ’s p a ra m e te r. H o w e v e r, th e se v a ria b le s are o ften stro n g ly c o rre la te d w ith
s e d im e n t c h a ra c te ristic s. F o r e x a m p le , in o n e stu d y (nr. 14) th e P e a rso n c o rre la tio n c o e ffic ie n t b e ­
tw ee n b e a c h slo p e an d m e a n p a rtic le siz e w as 0 .9 9 (as w e c a lc u la te d on b a s is o f th e d a ta p re se n te d ).
In a n o th e r s tu d y (nr. 24 ) th is c o e ffic ie n t a p p e a re d to b e e q u a l to 0 .7 8 . T h is in te rd e p e n d e n c y b e ­
tw e e n e n v iro n m e n ta l v a ria b le s , w h ic h is u su a lly e n c o u n te re d in fie ld stu d ie s, m a k e s it a lm o st im ­
p o ssib le to be c o n c lu s iv e o n th e m e c h a n ism s u n d e rly in g th e o b s e rv e d c o rre la tio n s. O b se rv a tio n a l
s tu d ie s lik e w e are c o n c e rn e d w ith in th e p re se n t stu d y , sh o u ld re p o rt th e se in te rd e p e n d e n c ie s . Y et,
o n ly o n e s tu d y (V a n d e r M e e r 1991) e x p lic itly d e s c rib e d th e se in te rd e p e n d e n c ie s b e tw e e n a b io tic
v a ria b le s. A n o th e r p o in t o f c o n c e rn is th a t stu d ies w e re u s u a lly sile n t on th e re a so n s o f in c lu d in g
sp e c ific a b io tic v a ria b le s in th e stu d y .
The scope o f benthos-environment regression models
F in a lly , w e w ill fro m a m o re g en e ral p e rsp e c tiv e , d isc u ss th e a p p lic a b ility o f re g re s sio n m o d e ls re ­
la tin g b e n th o s to th e e n v iro n m e n t. S u rv e y s o f th e m a c ro b e n th o s o f s o ft-se d im e n ts are u s u a lly c o n ­
d u c te d o v e r a sh o rt tim e sp an . U su a lly , o n ly a sin g le su rv e y is p e rfo rm e d . A re th e se m o d e ls o n ly
re le v a n t to th e h e re a n d n o w o f th e stu d y ? T h is w o u ld m ean th a t th e m o d e ls c o u ld o n ly b e u se d fo r
in te rp o la tio n . O r are th e m o d e ls also ap p lic a b le in th e fu tu re , th e p a s t an d in o th e r a re a s ? T h is
w o u ld e n a b le s o m e so rt o f e x tra p o la tio n . T h e a n sw e r to th is q u e s tio n re la te s to th e b io lo g ic a l a s ­
s u m p tio n s th a t can o r c a n n o t be m a d e. F o r e x a m p le , w h a t c a n w e s a y a b o u t th e p re s u m e d in te ra c ­
tio n b e tw e e n tim e an d e n v iro n m e n t? In o th e r w o rd s w h a t ca n w e sa y a b o u t th e tim e -in v a ria n c e o f
th e re g re ssio n p a ra m e te rs?
S u rv e y s o f th e m a c ro b e n th o s o f so ft-se d im e n ts are u su a lly s n a p -sh o ts in tim e , b u t b e n th ic
c o m m u n itie s (p a rtic u la rly in th e e s tu a rin e e n v iro n m e n t) are k n o w n fo r th e ir la rg e te m p o ra l v a ria ­
tio n s in sp e c ie s a b u n d a n c e (B e u k e m a 1989, C o o s e n et al. 1994). T h e se v a ria tio n s m a y b e d u e to th e
v a g a rie s o f w e a th e r, w h ich h av e stro n g im p a c t o n th e re c ru itm e n t su c c e ss o f m a n y sp e c ie s (B e u ­
k e m a 1989). U n k n o w n v a ria tio n s in th e e n v iro n m e n ta l c o n d itio n s d u rin g th e p e la g ic p h a s e o f th e
la rv a e m a y also c o n trib u te to th e la rg e v a ria tio n s in re c ru itm e n t th a t are u s u a lly o b se rv e d . V a ria tio n
in re c ru itm e n t se e m s to h a v e stro n g in flu e n c e on th e s tru c tu re o f th e c o m m u n ity . T h u s, w h e n o n ly a
sin g le p o in t in tim e is c o n s id e re d , it m ig h t b e th a t at all sites in th e stu d y a re a th e o b s e rv e d a b u n ­
d a n c e o f a sp e c ie s is m u c h lo w e r th an th e lo n g -te rm a v e ra g e d en sity . A t o th e r tim e s th e o b s e rv e d
a b u n d a n c e c o u ld be m u c h h ig h e r at all sites. T im e p la y s a ro le, an d th e n o tio n o f a sin g le ‘tr u e ’ re ­
g re ssio n m o d e l th a t w o rk e d in th e p a st an d w ill w o rk in th e fu tu re , is th e n n o t tra c ta b le .
In c o n c lu sio n , it w o u ld be h ig h ly re c o m m e n d a b le th a t fu tu re stu d ies on th e g o o d n e s s -o f-fit o f
re g re ssio n m o d e ls re la tin g e s tu ra rin e b en th o s to its e n v iro n m e n t sh o u ld n o t o n ly c o n s id e r th e ro le o f
sp a tia l sc a le b u t th e e ffe c ts o f te m p o ral sc ale s as w ell.
ACKNOW LEDGM ENTS
T h is stu d y w as p a id b y R IK Z /R W S w ith in th e p ro je c t W O N S * IN R IC H T . W e th a n k J. G ra v e la n d ,
F. T w isk an d T. B u lt fo r c o m m e n ts on an e a rlie r v ersio n .
SELECTED PAPERS
A u ste n , M . C ., W a rw ic k , R. M . (1 9 8 9 ). C o m p a riso n o f u n iv a ria te an d m u ltiv a ria te a s p e c ts o f e stu a rin e m e io b e n th ic c o m m u n ity stru c tu re . E stu a rin e , C o a sta l an d S h e lf S c ie n c e 2 9: 2 3 -4 2
B a c h e le t, G ., M o n ta u d o u in , X . D ., D a u v in , J.-C . (1 9 9 6 ). T h e q u a n tita tiv e d istrib u tio n o f su b tid al
m a c ro z o o b e n th ic a s se m b la g e s in A rc a c h o n B ay in re la tio n to e n v iro n m e n ta l fa c to rs: a m u lti­
v a ria te a n a ly sis. E stu a rin e , C o a sta l a n d S h e lf S c ie n c e 4 2 : 3 7 1 -3 9 1
B u h l-M o rte n se n , L ., H 0 isæ te r, T . (1 9 9 3 ). M o llu sc fa u n a alo n g an o ffs h o re -fjo rd g ra d ie n t. M a rin e
E c o lo g y P ro g re ss S e rie s 97: 2 0 9 -2 2 4
C la rk e , K. R ., A in sw o rth , M . (1 9 9 3 ). A m e th o d o f lin k in g m u ltiv a ria te c o m m u n ity stru c tu re to e n ­
v iro n m e n ta l v a ria b le s. M a rin e E c o lo g y P ro g re ss S e rie s 92: 2 0 5 -2 1 9
De
G ee ,
A .,
D e k k e r,
R.
b o d e m s a m e n s te llin g
(1 9 8 7 ).
H et
v o o rk o m e n
van
m a c ro z o o b e n th o s
in
re la tie
in h et su b litto ra le g e d e e lte v an d e W e ste lijk e W a d d e n z e e .
to t
de
N IO Z
U n p u b lis h e d rep o rt
D efeo , O ., J a ra m illo , E ., L y o n n e t, A. (1 9 9 2 ). C o m m u n ity stru c tu re an d in te rtid a l z o n a tio n o f the
m a c ro in fa u n a on th e A tla n tic c o a st o f U ru g u a y . Jo u rn a l o f C o a sta l R e se a rc h 8: 8 3 0 -8 3 9
E llio tt, M ., O 'R e illy , M . G . (1 9 9 1 ). T h e v a ria b ility an d p re d ic tio n o f m a rin e b e n th ic c o m m u n ity p a ­
ra m e te rs. In E llio tt, M . an d D u c ro to y , J.-P . (ed s.), E C S A 1 9 S y m p o siu m , O lse n & O lse n , pp.
2 3 1 -2 3 8
E sse lin k , P ., V an B e lk u m , J. (1 9 8 6 ). D e v e rsp re id in g van d e z e e d u iz e n d p o o t N e re is d iv e rs ic o lo r en
de k lu u t R e c u rv iro s tra a v o s e tta in d e D o lla rd in re la tie to t ee n v e rm in d e rd e a fv a lw a te rlo z in g .
R W S -D G W G W A O 8 6 .1 5 5
G ee , J. M ., A u ste n , M ., D e S m e t, G ., F e rra ro , T ., M c E v o y , A ., M o o re , S ., V an G a u s b e k i, D ., V in c x ,
M ., W a rw ic k , R. M . (1 9 9 2 ). S o ft se d im e n t m e io fa u n a c o m m u n ity re sp o n se s to e n v iro n m e n ta l
p o llu tio n g ra d ie n ts in th e G e rm a n B ig h t an d at a d rillin g site o f f th e D u tc h c o a st. M a rin e
E c o lo g y P ro g re ss S e rie s 91: 2 8 9 -3 0 2
G ra y , J. S ., A sc h a n , M ., C a rr, M . R ., C la rk e , K. R ., G re en , R. H ., P e a rso n , T . H ., R o s e n b e rg , R .,
W a rw ic k , R. M . (1 9 8 8 ). A n a ly sis o f c o m m u n ity attrib u te s o f th e b e n th ic m a c ro fa u n a o f F rie rfjo rd /L a n g e s u n d fjo rd an d in a m e so c o sm ex p e rim e n t. M a rin e E c o lo g y P ro g re ss S e rie s 46:
151-165
H ay n e s, D ., Q u in n , G . P. (1 9 9 5 ). T e m p o ra l an d sp atial v a ria b ility in c o m m u n ity stru c tu re o f a sa n d y
in te rtid a l b e a c h , C a p e P a te rso n , V ic to ria , A u stralia. M a rin e an d F re s h w a te r R e se a rc h 4 6: 931 942
H o g u e , E. W ., M ille r, C. B. (1 9 8 1 ). E ffe c ts o f se d im e n t m ic ro to p o g ra p h y on s m a ll-s c a le sp a tia l
d is trib u tio n s o f m e io b e n th ic
n e m ato d e s. Jo u rn a l o f E x p e rim e n ta l
M a rin e B io lo g y
an d
E c o lo g y 53: 181-191
J a ra m illo , E. (1 9 9 4 ). P a tte rn s o f sp e c ie s ric h n e ss in sa n d y b e a c h e s o f S o u th A m e ric a . S o u th A fric a n
Jo u rn a l o f Z o o lo g y 29: 2 2 7 -2 3 4
J a ra m illo , E ., M c L a c h la n , A. (1 9 9 3 ). C o m m u n ity an d p o p u la tio n re sp o n se s o f th e m a c ro in fa u n a to
p h y sic a l fa c to rs o v e r a ra n g e o f e x p o s e d sa n d y b e a c h e s in S o u th -c e n tra l C h ile . E stu a rin e ,
C o a sta l an d S h e lf S c ie n c e 37: 6 1 5 -6 2 4
L e g e n d re , P ., T h ru sh , S. F ., C u m m in g s, V. J., D ay to n , P. K ., G ra n t, J., H ew itt, J. E ., H in e s , A. H .,
M c A rd le , B. H ., P rid m o re , R. D ., S c h n ie d e r, D. C ., T u rn e r, S. J., W h itla tc h , R. B ., W ilk in so n ,
M . R. (1 9 9 7 ). S p atia l stru c tu re o f b iv a lv e s in a san d fla t: S c a le an d g e n e ra tin g p ro c e sse s. J o u r­
nal o f E x p e rim e n ta l M a rin e B io lo g y an d E c o lo g y 2 16: 9 9 -1 2 8
L ie , U. (1 9 7 8 ). T h e q u a n tita tiv e d istrib u tio n o f b e n th ic m a c ro fa u n a in F a n a fjo rd e n , W e ste rn N o r­
w ay . S a rsia 63: 3 0 5 -3 1 6
M c la c h la n , A. (1 9 9 6 ). P h y sica l fa c to rs in b e n th ic ec o lo g y : e ffe c ts o f c h a n g in g sa n d p a rtic le siz e on
b e a c h fau n a . M a rin e E c o lo g y P ro g re ss S eries 131: 2 0 5 -2 1 7
M e ire , P. M ., S ey s, J. J., Y se b a e rt, T. J. , C o a se n , J. (1 9 9 1 ). A c o m p a riso n o f th e m a c ro z o o b e n th ic
d istrib u tio n an d c o m m u n ity stru c tu re b e tw e e n tw o e s tu a rie s in so u th -w e s t N e th e rla n d s. In
E llio tt, M . a n d D u c ro to y , J.-P . (ed s.), E C S A 1 9 S y m p o siu m , O lse n & O lse n , p p. 2 2 1 -2 3 0
M o o re , D . M . (1 9 7 8 ). S e a so n a l c h a n g e s in d istrib u tio n o f in te rtid al m a c ro fa u n a in th e lo w e r M e rse y
E stu a ry , U .K . E stu a rin e , C o a sta l an d M a rin e S c ie n c e 7: 117-125
N e tto , S. A ., L an a, P. C . (1 9 9 7 ). In te rtid a l zo n a tio n o f b e n th ic m a c ro fa u n a in a su b tro p ic a l sa lt
m a rsh an d n ea rb y u n v e g e ta te d flat (S E B rasil). H y d ro b io lo g ia 353: 1 7 1 -180
O u g , E. (1 9 9 8 ). R e la tin g sp e c ie s p a tte rn s an d en v iro n m e n ta l v a ria b le s b y ca n o n ic a l o rd in a tio n : an
a n a ly sis o f so ft-b o tto m m a c ro fa u n a in th e re g io n o f T ro m s0 , N o rth e rn N o rw a y . M a rin e E n v i­
ro n m e n ta l R e se a rc h 45: 29 -4 5
O u g , E ., N æ s, K ., R y g g , B. (1 9 9 8 ). R e la tio n sh ip b e tw e e n so ft b o tto m m a c ro fa u n a an d p o ly c y c lic
a ro m a tic h y d ro c a rb o n s (P A H ) fro m sm e lte r d isc h a rg e in N o rw e g ia n fjo rd s a n d c o a sta l w ate rs.
M a rin e E c o lo g y P ro g re ss S e rie s 173: 3 9 -5 2
P e a rso n , T . H ., R o s e n b e rg , R. (1 9 8 7 ). F east an d fam in e: S tru c tu rin g fa c to rs in m a rin e b e n th ic
c o m m u n itie s. In G ee , J. H . R . and G ille r, P. S. (ed s.) 2 7 th S y m p . B rit. E co l. S o c. A b e ry s t­
w yth. B la c k w e ll S c ie n tific P u b lic a tio n s, O x fo rd .
P o o re , G. C . , M o b le y , M . C . (1 9 8 0 ). C a n o n ic a l c o rre la tio n a n a ly sis o f m a rin e m a c ro b e n th o s su rv e y
data. Jo u rn a l o f E x p e rim e n ta l M a rin e B io lo g y a n d E c o lo g y 4 5 : 3 7 -5 0
R a ffa e lli, D ., B o y le, P. R ., D u n n e t, G . M . (1 9 8 6 ). T h e in te rtid a l m a c ro fa u n a o f N ig g B ay . S y m p o ­
siu m on th e M a rin e E n v iro n m e n t o f th e M o ray F irth 9 1 , A b e rd e e n (U K ), pp. 113-141
R a ffa e lli, D ., K a ra k a ssis, I., G a llo w a y , A . (1 9 9 1 ). Z o n a tio n sc h e m e s o n sa n d y sh o re s: a m u ltiv a ria te
a p p ro a c h . Jo u rn a l o f E x p e rim e n ta l M a rin e B io lo g y an d E c o lo g y 148: 2 4 1 -2 5 3
S o eta ert, K ., V in c x , M ., W itto e c k , J., T u lk e n s, M . (1 9 9 5 ). M e io b e n th ic d is trib u tio n an d n e m a tio d e
c o m m u n ity s tru c tu re in fiv e E u ro p e a n c o m m u n itie s. H y d ro b io lo g ia 3 11: 1 8 5 -2 0 6
S u n , B ., F le e g e r, J. W ., C a rn e y , R . S. (1 9 9 3 ). S e d im e n t m ic ro to p o g ra p h y an d th e s m a ll-s c a le sp a tia l
d istrib u tio n o f m e io fa u n a . Jo u rn a l o f E x p e rim e n ta l M a rin e B io lo g y a n d E c o lo g y 167: 7 3 -9 0
V an d e r M e e r, J. (1 9 9 1 ). E x p lo rin g m a c ro b e n th o s -e n v iro n m e n t re la tio n sh ip b y c a n o n ic a l c o rre la ­
tio n a n a ly sis. Jo u rn a l o f E x p e rim e n ta l M a rin e B io lo g y an d E c o lo g y 148: 1 0 5 -1 2 0
W a rw ic k , R. M . (1 9 7 1 ). N e m a to d e a s so c ia tio n s in th e E x e estu ary . Jo u rn a l o f th e M a rin e B io lo g ic a l
A sso c ia tio n o f th e U .K . 51: 4 3 9 -4 5 4
W h itla tc h , R. B. (1 9 8 1 ). A n im a l-s e d im e n t re la tio n sh ip s in in te rtid a l m a rin e b e n th ic h a b ita ts : so m e
d e te rm in a n ts o f d e p o s it-fe e d in g sp e c ie s d iv e rsity . Jo u rn a l o f E x p e rim e n ta l M a rin e B io lo g y
an d E c o lo g y 53: 31 -4 5
Z w a rts, L. (1 9 8 8 ). D e b o d e m fa u n a v an de F rie s-G ro n in g se w a d d e n k u st. R W S -R IJP F le v o b e ric h t
294
G ENERAL REFERENCES
B a rry , J. P ., D a y to n , P. K . (1 9 9 1 ). P h y sica l h e te ro g e n e ity an d th e o rg a n iz a tio n o f m a rin e c o m m u n i­
ties. In K o la s a , J. an d P ic k e tt, S. T. A . (ed s.) E c o lo g ic a l h e te ro g e n e ity . S p rin g e r-V e rla g , N e w
Y o rk , pp. 2 7 0 -3 2 0
B e u k e m a , J. J. (1 9 8 9 ). L o n g -te rm c h a n g e s in m a c ro b e n th ic a b u n d a n c e on th e tid a l fla ts o f th e
W e ste rn W a d d e n S ea. H e lg o lä n d e r M e e re su n te rsu c h u n g e n 4 3: 4 0 5 -4 1 5
B e u k e m a , J. J. (1 9 9 8 a). B e sta a n d e situ a tie b o d e m d ie re n W a d d e n z e e . In O o st, A . P ., E n s, B. J.,
B rin k m a n , A. G ., D ijk e m a , K. S ., E y sin k , W . D ., B e u k e m a , J. J., G u ssin k lo , H. J., V e rb o o m ,
B. M . J. an d V e rb u rg h , J. J. (ed s.) In te g ra le b o d e m d a lin g sstu d ie W a d d e n z e e . N e d e rla n d se
A a rd o lie M a a ts c h a p p ij, A sse n , pp. 133-144
B e u k e m a , J. J. (1 9 9 8 b ). E ffe c te n o p b o d e m fa u n a . In O o st, A. P ., E n s, B. J., B rin k m a n , A . G .,
D ijk e m a , K. S ., E y sin k , W . D ., B e u k e m a , J. J., G u ss in k lo , H. J., V e rb o o m , B. M . J. an d V e r­
b u rg h ,
J.
J.
(e d s.)
In te g ra le
b o d e m d a lin g sstu d ie
W addenzee.
M a a ts c h a p p ij, A sse n , pp. 2 9 2 -3 0 0
C o c h ra n , W . (1 9 7 7 ). S a m p lin g te c h n iq u e s (se c o n d ed .). W ile y , N ew Y o rk
N e d e rla n d s e
A a rd o lie
C o o s e n , J., S ey s, J., M e ire , P. M . , C ra e y m e e rsc h , J. A . M . (1 9 9 4 ). E ffe c ts o f s e d im e n to lo g ic a l an d
h y d ro d y n a m ic a l c h a n g e s in th e in te rtid al are a s o f th e O o s te rsc h e ld e e s tu a ry (S W N e th e rla n d s )
on d istrib u tio n , d e n s ity an d b io m a ss o f fiv e c o m m o n m a c ro b e n th ic sp e cie s: Spio martinensis
(M e sn il), Hydrobia ulvae (P e n n a n t), Arenicola marina (L .), Scoloplos armiger (M u lle r) an d
Bathyporeia sp. H y d ro b io lo g ia 2 8 2 /2 8 3 : 2 3 5 -2 4 9
D a n k e rs, N . , B e u k e m a , J. J. (1 9 8 3 ). D istrib u tio n a l p a tte rn s o f m a c ro z o o b e n th ic s p e c ie s in re la tio n
to so m e e n v iro n m e n ta l fac to rs. In W o lff, W . J. (ed s.) E c o lo g y o f th e W a d d e n S ea. B a lk e m a ,
R o tte rd a m , p p .6 9 -1 0 3
D a v ie s, P. T. , T so , M . K. S. (1 9 8 2 ). P ro c e d u re s fo r re d u c e d -ra n k re g re ssio n . A p p lie d S ta tistic s 31:
2 4 4 -2 5 5
F lac h , E. C . (1 9 9 6 ). D istrib u tio n o f Corophium at d iffe re n t sc ale s. S e n c k e n b e rg ia n a m a ritim a 27:
119-127
G au c h , H. G ., C h a se , G . B. (1 9 7 4 ). F ittin g th e G a u ss ia n c u rv e to e c o lo g ic a l d ata. E c o lo g y 55: 13771381
G au c h , H . G ., C h a se , G. B ., W h itta k e r, R. H. (1 9 7 4 ). O rd in a tio n o f v e g e ta tio n sa m p le s b y G a u ss ia n
s p e c ie s d istrib u tio n s. E c o lo g y 55: 1 3 8 2-1 3 9 0
H a ss e ll, M . P ., C o m in s, H . N . , M ay , R. M . (1 9 9 1 ). S p atia l s tru c tu re a n d c h a o s in in s e c t p o p u la tio n
d y n a m ic s. N a tu re 353: 2 5 5 -2 5 8
J o n g m a n , R. H. G ., T e r B ra a k , C . J. F. , V an T o n g e re n , O. F. R. (1 9 8 7 ). D a ta a n a ly sis in c o m m u n ity
an d la n d sc a p e e c o lo g y . P U D O C , W a g e n in g e n
L e g e n d re , P ., T h ru s h , S. F ., C u m m in g s, V. J., D a y to n , P. K ., G ra n t, J., H ew itt, J. E ., H in e s, A. H .,
M c A rd le , B. H ., P rid m o re , R. D ., S c h n e id e r, D . C ., T u rn e r, S. J.,
W h itla c h , R. B. , W ilk in so n , M . R. (1 9 9 7 ). S p atia l stru c tu re o f b iv a lv e s in a sa n d fla t: sc a le a n d g e n ­
e ra tin g p ro c e sse s. Jo u rn a l o f E x p e rim e n ta l M a rin e B io lo g y a n d E c o lo g y 2 16: 9 9 -1 2 8
L ev in , S. A. (1 9 9 2 ). T h e p ro b le m o f p a tte rn a n d sc a le in e c o lo g y . E c o lo g y 73: 1 9 4 3 -1 9 6 7
M c A rd le , B. H ., H e w itt, J. E . , T h ru sh , S. F. (1 9 9 7 ). P a tte rn fro m p ro c e ss: it is n o t as e a sy as it
lo o k s. Jo u rn a l o f E x p e rim e n ta l M a rin e B io lo g y an d E c o lo g y 2 16: 2 2 9 -2 4 2
M u rra y , J. D . (1 9 8 9 ). M a th e m a tic a l b io lo g y . S p rin g e r-V e rla g , H eid e lb e rg
O k u b o , A. (1 9 8 0 ). D iffu sio n a n d ec o lo g ic a l p ro b le m s: m a th e m a tic a l m o d e ls. S p rin g e r-V e rla g , H e i­
d e lb e rg
P a lm e r, M . W . (1 9 9 3 ). P u ttin g th in g s in ev e n b e tte r o rd er: th e a d v a n ta g e s o f c a n o n ic a l c o rre s p o n ­
d e n c e a n a ly sis. E c o lo g y 74: 2 2 1 5 -2 2 3 0
P h ip p s, M . J. (1 9 9 2 ). F ro m lo cal to glo b al: th e le sso n fo rm c e llu la r au to m ata. In D e A n g e lis, D. D.
L. an d G ro ss, L. J. (ed s.) In d iv id u a l-b a se d m o d e ls an d a p p ro a c h e s in ec o lo g y : p o p u la tio n s,
c o m m u n itie s an d e c o sy ste m s. C h a p m a n an d H all, N ew Y o rk , pp. 1 6 5-187
S c h n e id e r, D . C . (1 9 9 4 ). Q u a n tita tiv e ec o lo g y : sp a tia l an d te m p o ra l sc alin g . A c a d e m ic P re ss, S an
D ie g o
S c h n e id e r, D. C ., T h ru s h , S. F ., D a y to n , P. (1 9 9 7 ). S c a le -u p o f e c o lo g ic a l e x p e rim e n ts: d e n s ity
v a ria tio n in th e m o b ile b iv a lv e Macomona liliana. Jo u rn a l o f E x p e rim e n ta l M a rin e B io lo g y
an d E c o lo g y 2 1 6 :1 2 9 - 1 5 2
T e r B raa k , C . J. F. (1 9 8 5 ). C o rre sp o n d e n c e an a ly sis o f in c id e n c e an d a b u n d a n c e d ata: p ro p e rtie s in
te rm s o f a u n im o d a l re sp o n se m o d el. B io m e tric s 4 1: 8 5 9 ,8 7 3
T e r B ra a k , C . J. F. (1 9 8 6 ). C a n o n ic a l c o rre sp o n d e n c e an a ly sis: a n ew e ig e n v e c to r te c h n iq u e fo r
m u ltiv a ria te d ire c t g ra d ie n t an a ly sis. E c o lo g y 67: 1 1 6 7 -1 1 7 9
T e r B raa k , C . J. F. (1 9 9 4 ). C a n o n ic a l c o m m u n ity o rd in a tio n . P art I: b asic th e o ry an d lin e a r m e th ­
o d s. E c o s c ie n c e 1: 1 2 7 -1 4 0
T e r B raa k , C . J. F. , P re n tic e , I. C . (1 9 8 8 ). A th e o ry o f g ra d ie n t an a ly sis. A d v a n c e s in E c o lo g ic a l
R e se a rc h 18: 2 7 1 -3 1 7
T so , M . K .-S . (1 9 8 1 ). R e d u c e d -ra n k re g re ssio n an d c a n o n ic a l an a ly sis. Jo u rn a l o f th e R o y a l S ta tis ­
tical S o c ie ty B 43: 183-189
V an d e r M e e r, J. (1 9 9 1 ). E x p lo rin g m a c ro b e n th o s -e n v iro n m e n t re la tio n s h ip b y c a n o n ic a l c o rre la ­
tion a n a ly sis. Jo u rn a l o f E x p e rim e n ta l M a rin e B io lo g y an d E c o lo g y 148: 1 0 5 -1 2 0
V an d e r M e e r, J. (1 9 9 7 ). A h a n d fu l o f fea th ers. G ro n in g e n S tate U n iv e rsity , G ro n in g e n
V an d e r M e er, J. (1 9 9 9 ). K e e p in g th in g s in order: m u ltiv a ria te d ire c t g ra d ie n t a n a ly sis o f a stro n g ly
flu c tu a tin g b e n th ic c o m m u n ity . Jo u rn a l o f S e a R e se a rc h 42: 2 6 3 -2 7 3
W h itta k e r, R. H. (1 9 6 7 ). G ra d ie n t an a ly sis o f v e g e ta tio n . B io lo g ic a l R e v ie w s 4 2: 2 0 7 -2 6 4
W ie n s, J. A . (1 9 8 9 ). S p atia l sc a lin g in e c o lo g y . F u n c tio n a l E c o lo g y 3: 3 8 3 -3 9 7
NIOZ-RAPPORT 1999-7
TABLE OF CONTENTS
ABSTRACT
3
INTRODUCTION
4
MATERIAL AND METHODS
9
RESULTS
10
DISCUSSION
16
ACKNOWLEDGMENTS
18
SELECTED PAPERS
19
GENERAL REFERENCES
21