The paleoecological significance of diversity: The effect of time averaging and differential preservation on macroinvertebrate species richness in death assemblages

Palaeogeography, Palaeoclimatology, Palaeoecology, 63 (1988): 73-89

73

Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

THE PALEOECOLOGICAL SIGNIFICANCE OF DIVERSITY: THE EFFECT OF TIME AVERAGING AND DIFFERENTIAL PRESERVATION ON MACROINVERTEBRATE SPECIES RICHNESS IN DEATH ASSEMBLAGES G. M. S T A F F a n d E. N. POWELL

Department of Geology, Department of Oceanography, Texas A&M University, College Station, TX 77843 (U.S.A.) (Received July 21, 1987)

Abstract Staff, G. M. and Powell, E. N., 1988. The paleoecological significance of diversity: the effect of time averaging and differential preservation on macroinvertebrate species richness in death assemblages. Palaeogeogr., Palaeoclimatol., Palaeoecol., 63: 73-89. The effect of time averaging on species richness of the preservable component (animals with preservable hard parts) of living benthic communities was investigated using long-term (24-30 mo) data sets obtained by recurrent sampling in estuarine and euhaline (30 40 ppt) habitats. About 20-40% of all living species collected were preservable. Species richness of the living community increased with increasing salinity and water depth. Cumulative species richness increased with increasing duration of study. The percentage of preservable species, however, declined with increasing depth. As many preservable species were collected over time in some physically variable estuarine habitats as were collected in the physically less variable, euhaline habitats. Changing environmental factors allowed different species to inhabit these estuarine areas as time passed, whereas species richness was usually higher in euhaline habitats at any particular time. Hence, species richness in the death assemblage and subsequent fossil assemblage may be as high in some physically variable, estuarine habitats as in more invariant euhaline habitats. The species composition of the preservable component of the living community was more persistent than the nonpreservable component. That is, on the average, species additions or replacements occurred more frequently in the nonpreservable component. This increased persistence of the preservable component, however, could not offset the inherently more rapid temporal changes in faunal composition that occurred in physically variable habitats. Therefore, the classic ecologic relationship between increased species richness and reduced environmental variability may not be preserved. Additional evidences must be used to distinguish between species-rich assemblages produced by time averaging of noncontemporaneous taxa in environmentally variable habitats and those produced by diverse communities in less variable habitats.

Introduction Diversity measures, from simple species richhess to more complex d i v e r s i t y indices, h a v e b e e n used with v a r y i n g degrees of success by most ecologists and paleoecologists. Although t h e e c o l o g i c a l u s e a n d s i g n i f i c a n c e of d i v e r s i t y a r e c o n t r o v e r s i a l ( G o o d m a n , 1975; R h o d e , 1978; O s m a n a n d W h i t l a t c h , 1978; L a m b s h e a d e t al., 0031-0182/88/$03.50

1983), t h e b a s i c c o n c e p t of d i v e r s i t y is w i d e l y used a n d accepted. The c o n c e p t of diversity, p a r t i c u l a r l y t h e r e l a t i o n s h i p of d e c r e a s i n g diversity with increasing environmental stress ( s e n s u S a n d e r s , 1968) o r d e c r e a s i n g e n v i r o n m e n t a l v a r i a b i l i t y (e.g. B o e s c h a n d R o s e n b e r g , 1981), h a s a l s o b e e n u s e d i n p a l e o e c o l o g y (e.g. H i c k e y a n d Y o u n k e r , 1981; V a l e n t i n e , 1984; F f i r s i c h a n d O s c h m a n n , 1986; F f i r s i c h a n d

© 1988 Elsevier Science Publishers B.V.

74 Werner, 1986). The exact paleoecological interpretation of diversity as an attribute of the paleocommunity is not always clear (Lasker, 1976; Peterson, 1977), however, because: (1) not all individuals are preserved and those that are may be transported from the site of death (e.g. Valentine and Mallory, 1965; Bosence, 1 9 7 9 ; Powell et al., 1982); (2) time averaging (in the case of the paleocommunity, the postmortem mixing of individuals living at different times) can produce a fossil assemblage comprising a montage of community attributes from many generations (Staff et al., 1986 discuss the various types of timeaveraging), Diversity typically comprises measures of species richness and evenness. Differential preservation of species and size classes, even among preservable taxa (those living species having preservable hard parts), makes accurate preservation of evenness improbable (Cummins et al., 1986a, b). Consequently, the term diversity in paleoecology usually refers solely to species richness (e.g. Valentine, 1971). Although many taxa have no hard parts and, hence, are rarely preserved (Stanton, 1976; Schopf, 1978), some individuals of nearly all preservable taxa are preserved (e.g. Warme, 1969; Warme et al., 1976; Staff et al., 1986). Consequently, in fossilassemblagesunaffected by diagenetic alteration (e.g. Koch and Sohl, 1983), species richness may represent a real community attribute, rather than a product of taphonomy as, for example, most size-frequency distributions appear to be (Cummins et al., 1986b). Lasker (1976), Peterson (1977) and Carthew and Bosence (1986) pointed out that, second only to the non-preservation of soft-bodied taxa, the postmortem mixing of noncontemporaneous taxa produced the gravest error in interpreting species richness as a community attribute. The accumulation of noncontemporaneous taxa increases species richness in the fossil assemblage beyond what was present at any specified time in the living community. In fact, species richness of the fossil assemblage will always be greater than that of the preservable component of the living community at any one time. Yet, at the same

time, species richness of the fossil assemblage will always be less than the cumulative total of all preservable and non-preservable taxa that lived in the community while the death assemblage was formed (Peterson, 1977; McCall and Tevesz, 1983; Staff et al., 1986). Consequently, Staff et al. (1986) suggested that the species richness of a death assemblage formed in a physically variable habitat may be relatively high because of substantial species replacement in the living community over time. Potentially, then, the classic relationship between species richness and environmental variability typically found, for example, along estuarine-euhaline gradients (Boesch, 1977) might not be adequately preserved in the fossil record. Testing such an hypothesis requires long-term studies of communities and their death assemblages. Because essentially all species with preservable hard parts will be preserved, the number of preservable species living in a community can provide a minimal estimate of species richness in the death assemblage. Accordingly, long-term studies of benthic communities can provide a minimal estimate of the effect of time averaging on species richness that might be used to examine the meaning of species richness in the fossil record. Thus, we examined the impact of time averaging on species richness by examining rates of species replacement in benthic communities from estuarine, lagoonal, and continental shelf habitats. Specifically we asked three questions. (1) What percentage of the living community's taxa are preservable? (2) Is the preservable component more or less persistent (temporally invariant) than the remaining species? (3) In environmentally variable habitats, can changes in species composition in the living community increase species richness in the time-averaged death assemblage so that the relationship of species richness and environmental variability is poorly preserved? The d a t a We originally sought studies where frequent (monthly in most cases) recurrent sampling

75 was conducted over many years and in which essentially all taxa were identified to species, Such data being rarely published in sufficient detail, we requested original data sets from research groups t h a t were involved in recurrent sampling programs over the last decade. We considered only soft-bottom benthic habitats. Most studies t h a t we used were of 24-30mo duration; hence, for comparative purposes, we used only the last ~ 30 mo of data from longer-term records. The data sets used were: (1) Mass~'s (1972b) data for the Mediterranean Coast of France; (2) data for Chesapeake Bay collected by A. F. Holland and coworkers (see Holland, A.F., 1985; Holland, A.F. et al., 1985 for further consideration of these data); (3) data for Copano Bay, Aransas Bay and Corpus Christi Bay, Texas collected by the Texas Water Development Board (see Holland, J. S. et al., 1973; 1974); (4) data for the mid-Atlantic continental shelf of the eastern United States collected by D.F. Boesch and others (discussed further by Boesch, 1979). Study lengths and site descriptions are tabulated in Table I. We take this opportunity to t h a n k Drs. A. F. Holland, D. F. Boesch, and the Texas Water Development Board for making their data available, when many others that we contacted declined, We supplemented these data with other studies of shorter duration and/or less frequent sampling that were available in the literature (Table II). Here we echo the lament of Platt and Lambshead (1985) on the infrequent reporting of data on community composition in the published literature. Many otherwise excellent studies could not be used because the reported data were not sufficiently complete. The tabulation in Table II represents the first ~ - 6 0 satisfactory data sets that we encountered. We make no claim to an exhaustive search of the literature, Following Staff et al. (1985), we defined preservable biota as shelled molluscs, brachiopods, serpulid and spirorbid worms, calcitic sponges, hard bryozoans, barnacles, and echinoids. Molluscs dominated the preservable fraction of most of the assemblages; hence, in

large measure, the analyses address the importance of Mollusca in benthic communities. Microfauna and meiofauna, which were tabulated in some data sets, were not used. Because size ranges were rarely given, we defined '~meiofauna" taxonomically after Powell et al. (1986)rather than by size (e.g. McIntyre, 1969) and, consequently, excluded nematodes, turbellarians, copepods, etc. Statistical analyses are discussed where appropriate in the following sections. Results and discussion

Species richness and preservability Johnson (1964) observed that about 30% of the species in benthic communities are preservable. The compilations in Tables I and II agree. About 20-40% of the taxa are preservable in most benthic communities. Data in Tables I and II were analyzed using a multiple analysis of covariance (MANCOVA). Dependent variables were species richness and the percentage of all species collected over the study's duration t h a t were preservable. Independent variables were substratum, salinity, depth, and sampling duration. Substrata were divided into four categories; viz. gravel, sand, muddysand/sandy-mud, and mud. Salinity was divided into categories using the Venice system; viz. oligohaline (0.5-5 ppt), mesohaline (5-18ppt), polyhaline (18-30 ppt), euhaline (30-40 ppt). Following Boesch's (1977) arguments on the importance of periods of low salinity in determining community composition along estuarine gradients, we assigned studies to these categories according to the lowest, rather than the mean, salinity reported. Species richness was not significantly affected by substratum ( P > 0.05). Species richness increased significantly with increasing salinity (P = 0.005, Table II; P < 0.0001, Table I; P < 0.0001, Tables I and II combined), following the well-known trend of diversity change along the estuarine-euhaline gradient. Typically 20-40 species were encountered at mesohaline

76 sites d u r i n g 2 y r of sampling, w h e r e a s m o r e t h a n 150 species were u s u a l l y e n c o u n t e r e d at e u h a l i n e sites. As expected, species r i c h n e s s i n c r e a s e d s i g n i f i c a n t l y with i n c r e a s i n g d e p t h (Table I, P = 0 . 0 1 ; T a b l e II, P < 0 . 0 3 ) . N o r m a l l y , over 200 species w e r e e n c o u n t e r e d o v e r 2 y r s a m p l i n g at c o n t i n e n t a l shelf sites ( > 5 0 m ) , w h e r e a s the t a k e r a r e l y exceeded 100 species at s h a l l o w w a t e r sites ( < 5 m). The d u r a t i o n of the s a m p l i n g p r o g r a m , in essence the a m o u n t of time a v e r a g i n g e n c o m p a s s e d by c u m u l a t i n g samples over time, also s i g n i f i c a n t l y affected species richness ( P = 0.003, T a b l e II; P < 0.0001, Tables I a n d II combined). The l o n g e r the s a m p l i n g p r o g r a m , the m o r e species were e n c o u n t e r e d (e.g. F i g s . l - l l ) . Thus, species r i c h n e s s was affected p r i n c i p a l l y by salinity, depth, a n d s a m p l i n g d u r a t i o n , The p e r c e n t a g e of p r e s e r v a b l e species was n o t affected s i g n i f i c a n t l y by s u b s t r a t u m or s a m p l i n g d u r a t i o n (P>0.05), b u t was affected significantly by s a l i n i t y ( P = 0 . 0 2 , Table II; P = 0.07, Tables I and II combined) and d e p t h ( P = 0 . 0 5 , Table II; P = 0 . 0 0 0 1 , Tables I a n d II combined). As d e p t h increased, t h e p r o p o r t i o n of p r e s e r v a b l e t a x a decreased. N o r m a l l y less t h a n 25% of all species were p r e s e r v a b l e at sites below 50 m, w h e r e a s at sites s h a l l o w e r t h a n 10 m, 3 0 - 5 0 % of all species h a d preserv-

Mid-Atlantic Continental Shelf 190~80170160" 15014013c12o11s10o908o70605040- j _ _ _ . - ¢ - - - - - ~ 302o~0--,11 . . . . .2. . . . . . . . 6. . . . .8. . . . 11 2 5 SamplingDates 2OO

_~_.o_._._.o_._~B,

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Fig.2. Cumulative number of species collected with time for selected stations on the mid-Atlantic continental shelf. Upper two curves depict the cumulative number of all speciesencountered. Lower two curves depict the cumulative number of preservable species encountered. Stations are described in more detail in Table I.

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Sampling Dates Fig.1. Cumulative number of species collected with time for selected stations on the mid-Atlantic continental shelf, Upper three curves depict the cumulative number of all species encountered. Lower three curves depict the cumulative number of preservable species encountered. Stations are described in more detail in Table I.

able h a r d parts. In c o n t r a s t , as salinity increased, the p r o p o r t i o n of p r e s e r v a b l e t a x a increased. The r e l a t i o n s h i p of the p r o p o r t i o n of p r e s e r v a b l e t a x a and salinity was due solely to a h i g h e r p e r c e n t a g e of p r e s e r v a b l e species at e u h a l i n e sites ( P = 0.22 for all lower salinities). In c o n t r a s t , the r e l a t i o n s h i p b e t w e e n the p e r c e n t a g e of p r e s e r v a b l e species and d e p t h was m u c h s t r o n g e r at these and all o t h e r sites

77

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Fig.6. Cumulative number of species collected with time for selected stations in Chesapeake Bay. Upper three curves depict the cumulative number of all species encountered. Lower three curves depict the cumulative number of preservable species encountered. Stations are described in more detail in Table I.

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Fig.5. Cumulative number of species collected with time for selected stations in Chesapeake Bay. Upper three curves depict the cumulative number of all species encountered. Lower three curves depict the cumulative number of preservable species encountered. Stations are described in more detail in Table I.

Fig.7. Cumulative number of species collected with time for selected stations in Chesapeake Bay. Upper three curves depict the cumulative number of all species encountered. Lower three curves depict the cumulative number of preservable species encountered. Stations are described in more detail in Table I.

(P < 0.0001 vs. P = 0.01 for all other sites, Tables I and II combined). Hence, depth, rather than salinity, was the primary factor affecting the proportion of all taxa that were preservable, Thus, the analysis suggests that, in situations where depth and salinity are significantly correlated (as might be the case for estuarinecontinental shelf transects), the trend of in-

creasing species richness with increasing salinity might be offset to a great degree by a tendency for the proportion of preservable species to decline. Indeed, the number of preservable species at continental shelf sites was frequently no greater than at estuarine sites despite the much higher total species richness on the shelf (Tables I and II). Consequently, the expected changes in species rich-

141-1 104-2 [104-6] 120-3 [100-2] 115-5

{127-2} 127-6 151-2 122-6 122-1 122-2 127-3 131-2 147-5 [200-2] [147-3] 152-2 147-1 142-1 142-6 142-2

Aransas Bay

Corpus Christi Bay

6 13 30 [43]

44-2 54-3 54-1

Copano Bay

Chesapeake Bay

[38-2] 53-2 53-4

Station

Nueces Bay

Location

2 2 2 2

4 4 3 3 3 3 4 4 3 2 3 4 3 4 4 4

4 4 4 4 4 4

3 3 2

3 4 4

Substrate

2 2 2 2

1 3 3 3 3 2 3 3 3 2 3 3 3 3 3 3

3 2 2 2 2 2

2 2 2

1 3 4

Salinity

2 3 2-3 2-3 2-3

3 4 1 3 2 4 2 3 <1 2 2 2 3 3 5 4

2 1 2 3 1 1

1 1 1

<1 1 < 1

Depth (m)

32 32 32 32

32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32

32 32 32 32 32 32

30 32 32

30 32 32

Duration (too)

0.3 0.3 0.2 0.2

14.7 4.0 4.4 17.6 3.4 4.0 8.6 4.3 6.8 3.5 17.6 22.0 11.5 3.1 4.3 4.4

9.4 4.3 5.9 1.8 3.0 3.1

1.5 3.3 1.3

4.3 2.8 2.3

Number of preservable taxa per sampling

10.5 9.3 9.9 8.7

27.0 9.8 5.8 27.7 7.6 9.0 17.1 8.2 10.8 11.7 31.5 35.7 19.3 5.7 8.8 8.1

14.6 4.9 12.0 5.0 7.5 8.0

3.6 7.3 3.2

9.3 7.7 5.6

N u m b e r of nonpreservable taxa per sampling

35 30 37 21

188 66 124 203 102 51 135 91 159 232 208 283 196 85 62 76

153 69 94 36 64 58

63 84 47

86 66 47

Species richness (total community)

10 9 9 8

63 23 42 76 35 17 37 32 53 41 83 104 64 24 21 24

53 26 33 14 32 19

27 32 23

38 21 16

Species richness (preservable component)

D a t a for t h e 4 l o n g - t e r m s t u d i e s d e s c r i b e d in t h e D a t a s e c t i o n . Salinity: 1, o l i g o h a l i n e ; 2, m e s o h a l i n e ; 3, p o l y h a l i n e ; 4, e u h a l i n e . S u b s t r a t e : 1, gravel; 2, s a n d ; 3, s a n d y m u d / m u d d y s a n d ; 4, mud. V a l u e s in b r a c k e t s r e p r e s e n t d a t a s e t s w h e r e i n t h e r a t e o f n e w s p e c i e s e n c o u n t e r s w i t h t i m e w a s h i g h e r in t h e p r e s e r v a b l e c o m p o n e n t ; braces r e p r e s e n t c a s e s w h e r e t h e r a t e w a s e q u i v a l e n t in t h e p r e s e r v a b l e a n d n o n p r e s e r v a b l e c o m p o n e n t

TABLE I

[B1] [B2] B3 [B4] E2 [E4]

A1 [A4] F2 F3 F4

Outer Shelf

Shelf Break

[1] [2] 3

C4 D1

Central

Camargue Coast

C2

Continental Shelf

2 2 2

2 3 3 3 2

2 2 2 2 2 2

2 2

2

4 4

52 [54]

Inner

2 2 2 2 2 3 3 4 4 4 4 4 4 4 4

45 {47} 49 51 [53] 26 31 10 {20} {32} 34 44 46 48 50

4 4 4

4 4 4 4 4

4 4 4 4 4 4

4 4

4

2 2

2 2 2 2 2 2 2 2 2 2 2 2 2 2 2

5 6 7

90-201 90 201 90 201 90-201 90-201

40 66 40-66 72-74 44-66 44-66 64-94

34 51 31-39

15-29

10-12 10 12

2-3 2-3 2 3 2 3 2-3 6-7 6-7 10-12 10-12 10 12 10-12 10-12 10-12 10-12 10-12

28 28 28

23 23 16 13 13

22 22 22 22 17 17

23 23

22

29 29

32 32 32 32 32 29 29 29 29 29 29 29 29 29 29

13.8 16.7 16.3

38.9 27.1 20.0 22.1 18.5

16.6 12.5 24.1 11.1 30.0 36.5

15.8 9.5

9.3

0.2 0.4

0.2 0.2 0.2 0.5 0.4 0.3 0.3 0.2 0.2 0.2 0.0 0.2 0.2 0.1 0.2

33.6 38.0 36.5

76.5 72.3 59.5 61.9 71.8

68.6 67.7 84.0 52.5 84.6 83.4

35.4 39.7

32.3

5.8 8.3

9.1 9.3 9.6 11.0 12.0 12.6 12.8 7.0 7.1 7.1 8.1 7.1 7.2 7.3 7.4

89 100 105

285 270 229 256 225

281 180 246 169 257 269

192 200

161

21 25

27 21 22 24 31 32 37 18 19 16 22 19 20 19 19

35 38 34

72 50 55 64 52

49 30 56 28 61 75

47 29

30

5 11

7 6 6 12 12 9 10 6 7 6 1 6 6 4 5

Location

Tampa Bay, Florida Tampa Bay, Florida Tampa Bay, Florida Buchanan and Warwick Off Northumberland, (1974) England Day et al. (1971) North Carolina shelf North Carolina shelf North Carolina shelf Dexter (1978) Off Imperial Beach, California Edwards (1973) Las Maritos, Venezuela San Luis, Venezuela Gage (1972) Loch Creran, Scotland Loch Creran, Scotland Loch Etive, Scotland Firth of Lorne, Scotland Gomez (1981) Ebrie Lagoon, Ivory Coast Guelorget and Prevost Lagoon, Michel (1979) France Prevost Lagoon, France Prevost Lagoon, France Prevost Lagoon, France Holm (1978) Florida Keys Florida Keys Florida Keys Holme (1949) River Exe estuary, England Holme (1953) English Channel

Bloom et al. (1972)

Source

4 4

2 4

4 4 4 4 4

3 3 3 3 3 3

Station 12

Average of stations 1-100, II + 3, IV ÷ 3, VI + 3 Average of stations A6-7, B4-7, C4-6

1

3

Station 4

1

1

3

Station 11

2

1

1

4

3

4

4

Average of 3 stations

Station 3

4

3

Average of 2 stations

4

4

2

mean of 4 transects

4 4 4 4

2 2 3 2

Average of 5 stations Average of 3 stations

3 3 3 4

Salinity

2 2 2 4

Substrate

Transect 1 Transect 2 Transect 3 June, 1971 sample

Comments

Additional data tabulated from the literature. Explanation of salinity and substrate is given in Table I

TABLE II

40-70

1 1 1 0

1

1

1

1

7

20-150

20 150

20-150

20-150

0

0

0-20 40-120 160-200 3-7.5

0 0 0 8

Depth (m)

single

2 samples 2 samples 2 samples single

18 mo

18 mo

18 mo

18 mo

14 mo

single

single

single

single

single

single

9 mo 9 mo 9 mo 1 yr

7 mo 7 mo 7 mo single

Duration

63

112 107 87 48

20

23

18

23

70

63

155

234

88

47

65

103 122 80 131

30 40 49 66

Species richness (all species)

34.9

51.7 54.2 43.7 22.9

15.0

21.7

11.1

21.7

30.0

21.0

21.9

26.4

26.1

29.8

43.1

17.1 21.3 27.5 28.2

40.0 30.0 36.7 10.6

Species preservable (% of total)

oo

Persson (1982)

Moore et al. (1968) Pearson (1970)

Maurer and Aprill (1979) McIntyre and Eleftheriou ( 1 9 6 8 ) McNulty et al. (1962)

Maurer (1977)

Mass~ (1972a)

Mass~ (1971b)

Mass~ (1971a)

Hutchings et al. (1978) Ivell (1981) Lewis and Stoner (1983)

Walis Lake Smiths Lake Limfjord, Denmark Apalachee Bay, Florida Apalachee Bay, Florida Bay of Bandol, France Bay of Bandol, France Bay of Bandol, France Gulf of Marseille, France Gulf of Marseille, France Verdon Bay, France Verdon Bay, France Fos Gulf, France Rehoboth Bay, Delaware Indian River, Delaware Cape Henlopen, Delaware Bay Firemore Bay, Scotland Biscayne Bay, Florida Biscayne Bay, Florida Biscayne Bay, Florida Biscayne Bay, Florida Lochs Linnhe and Eil, Scotland Lochs Linnhe and Eil, Scotland Lochs Linnhe and Eil, Scotland Lochs Linnhe and Eil, Scotland H a n s Bight, Baltic H a n s Bight, Baltic Han5 Bight, Baltic Average of stations 10, 11, 53, 24 Average of stations 36, 37, 39, 42 Average of stations 5, 6, 3, 7, 22 Average of stations 27, 8, 19

Average of 5 transects

4 4

2 2

3 3

2 1

2 2 2

3

3

2 2 4

3

4

3

4

2

4

3

2

3

2

3 2

4 4 4 3

2 3 4

4

2

4 4

2

Station 3

4

4

3

3 3 3 3

2

2

Station 2

Average of Stations 1, 2 Average of Stations A, B, C Station 1 Station 2

2

2

Seagrass Bed Station 1

4 4 2 2

Average of 9 stations Average of 2 stations

5 39 40 59 60 80

14

24

22

82

0

3

3

3

1

0

2

3 9 1• 2

2

5

11

7

5

2

8 5 15 2

single single single

4 yr

4 yr

4 yr

4 yr

single

single

single

single

3 mo

2 yr

2 yr

40 mo 40 mo 72 mo 2 yr

12 mo

37 mo

24 mo

24 mo

35 mo

single

single single 13 mo single

21 18 12

136

170

104

100

55

33

93

41

146

26

126

108 106 81 117

41

92

103

92

113

80

67 21 40 38

23.8 22.2 16.7

27.9

26.1

27.8

17.0

20.0

48.5

47.3

52.5

19.0

38.5

34.1

32.4 32.1 42.0 37.6

21.9

29.3

34.9

29.3

31.0

14.2

31.3 42.8 47.5 10.5

G u n n a m a t t a Bay, Australia Biscayne Bay, Florida Biscayne Bay, Florida Biscayne Bay, Florida Long Island Sound Long Island Sound Buzzards Bay, Massachusetts Barnstable Harbor, Massachusetts County Down, Ireland Bramble Bay, Australia Moreton Bay, Australia Apalachee Bay, Florida Lynher Estuary, England C a r m a r t h e n Bay, England Cape Cod Bay, Massachusetts Cape Cod Bay, Massachusetts Cape Cod Bay, Massachusetts

Rainer (1982)

Subrahmanyam and Coultas (1980) Warwick and Price (1975) Warwick et al. (1978) Young and Rhoads (1971)

Sanders et al. (1962) Seed and Lowry (1973) Stephenson (1980)

Sanders (1960)

Sanders (1956)

Rosenberg (1975)

Location

Source

TABLE II (continued)

3 3

4 2 3

Station 4 Average of 3 stations, Ampelisca community (Sanders, 1968) Average of 3 stations Nepthys Nucula community

Average of stations 2318, 2118, 1918 Average of stations 1718, 1518 Average of stations 1118, 0918

3 3 3

3 4

4

4 2

2

4

4

2

Average of 3 stations

3

2

2

Average of 3 stations

3

3

4

4

2

Average of 7 locations

Marsh

2

Average of 6 stations

4

4

3 4

4

4

Salinity

2

2

Substrate

Average for entire bay Average of stations ~1 and 3 Station 2

Comments

34-42

20-26

10-20

10-17

0

0

4-6

1-3

0

0

15

11-30

6-23

3 4

3 4

3-4

0 8

Depth (m)

single

single

single

13 mo

2 yr

2 yr

3.5 yr

3.5 yr

4 mo

single

2 yr

13 mo

13 mo

single

single

single

single

Duration

35

37

47

57

11

52

117

82

16

69

95

39

64

29

37

35

40

Species richness (all species)

22.8

18.9

44.6

33.3

54.5

28.8

18.8

22.0

13.7

24.6

27.4

38.5

31.2

27.5

43.2

25.7

20.0

Species preservable (% of total)

83 Aransas Bay 160~

.

.

.

.

300.

152-2

140

260 ~

130

240

20 /

!I

11o-4 lOO7

1 4e o-

U~ t '~ gO

220~

147-3

~ 200G 1

147-1

O9 180~ 140 ~

~, 70

120 3

60/

~ 120-

152-2

Z

147-3 47-

_

104-6 t20-3

30 20 lO O

9

~

11

1

T I I 3 5

7

~

E [ [ I 9 11 1 3 Sampling Dates

I F I r I [ I ] T 5 7 9 11 1 3 5

I I I IT 11 1

I I [ I~1 3 5 7

I I [-] ] ] [ ~ I I [ I f I ] ] I T I I I I 9 11 1 3 5 7 9 11 1 3 5 Sampling Dates

Camargue Coast

130

170t 160 ,

120 110

1504 140! 130

1004

51-2

~oo4 90

~ 90-

"6 70J

~o! ~o~

~oo_ E=50-

60~ 504

Z

' 40~

404 30_{

3o28-

• •

20

l

10-

1~ i . . . . . . . . . . . . 9 11 I 3 5

7

9

- . . . . . . . . . . . . . . . . . . . 11 I 3 5 7 9 11 Sampling

Fig.9.

9

~vV

Fig.t0. Cumulative number of species collected with time for selected stations in Corpus Christi Bay. Upper three curves depict the cumulative number of all species encountered. Lower three curves depict the cumulative number of preservable species encountered. Stations are described in more detail in Table I.

Corpus Christi Bay

190~

10080 68 ~

O]

Fig.8. Cumulative number of species collected with time for selected stations in Aransas Bay. Upper of each pair depicts the cumulative number of all species encountered, Lower of each pair depicts the cumulative number of preservable species encountered. Stations are described in more detail in Table I.

Z

Corpus Christi Bay

141mq]

Cumulative

number

of

I

3

5

7

Dates

species

0

, ~,

~ i ~,

~ i1,11

,1 i ~ i & , ~ , ~ i111 I ~ i ~ i ~ i ~ i ~ i111 I I Sampling

collected

with

for selected stations in Corpus Christi Bay. Upper three curves depict the cumulative number of all species encountered. Lower three curves depict the cumulative number of preservable species encountered. Stations are described in more detail in Table I.

ness across an estuarine-euhaline might not be well preserved,

Dates

time

Fig.ll. Cumulative number of species collected with time for selected stations from the Camargue Coast of France. Upper three curves depict the cumulative number of all species encountered. Lower three curves depict the cumu. lative number of preservable species encountered. Stations are described in more detail in Table I.

gradient

Species richness across the estuarine-euhaline gradient To confirm the trend that species richness of the preservable component does not change along the estuarine-euhaline gradient as strongly as species richness of the entire living

community, we analyzed only those sites from Tables I and II that had been sampled for > 2 yr in order to mitigate the effects of seasonality and short-term disturbance. In this compilation, species richness was significantly negatively correlated with the percentage of species that were preservable (Pearson's correlation, P=0.02). As expected, neither were significantly affected by study duration (MANCOVA,

84 P>0.05). Hence, these data were not encumbered by the trend of increasing cumulative species richness with sampling duration present in the entire data set. Cumulative species richness increased significantly with salinity and depth (MANCOVA, both P<0.0001), as would be expected for an estuarine-euhaline gradient. The percentage of the species that were preservable decreased significantly with depth (P= 0.006). Thus, species richness increased with increasing depth, but the proportion of species that were preservable decreased. As a result of these opposing trends, species richness of the preservable component increased substantially less than would be expected from observation of the entire living community along the estuarineeuhaline gradient.

Time averaging across the estuarine-euhaline gradient Two factors could affect preservation of what should be a relatively clear record of the estuarine-euhaline gradient in species richness, namely: (1) the above-discussed opposing trends in species richness and the relative proportion of preservable species; and (2) the effect of time averaging on the temporal replacement of species. Boesch (1977)described a classic example of the latter. The rate of species replacement in euhaline and, under certain conditions, oligohaline areas tends to be relatively low when compared to mesohaline and polyhaline areas because, as the haloclines move up-estuary and down-estuary with fluctuating freshwater input and saltwater exchange, the central region of the estuary will be exposed to a much more frequent and wider range of salinity change (Boesch et al., 1976; Boesch, 1977). Consequently, more species may live noncontemporaneously in the central portion of the gradient, thus enriching the species composition in the death assemblage above what would be expected from a single sampling of the living community. Staff et al. (1985, 1986) provided an example of such enrichment of a death assemblage formed in a normally mesohaline habitat.

We compared data from three salinity regimes using the compilation in Table I: viz., oligohaline, euhaline, mesohaline-polyhaline. In each case, we compared the mean number of preservable and nonpreservable organisms obtained at each sampling with their respective cumulative totals for the entire time-series of observations. We then calculated the average fraction of the total species encountered that were collected on each sampling occasion. The proportion of the total species, preservable or nonpreservable, collected per sampling occasion was lower in the mesohaline-polyhaline sites than the euhaline sites. All three salinity groupings were significantly different (Duncan's multiple range, ~=0.05; oligohaline > euhaline > mesohaline-polyhaline for the nonpreservable, 2=54%, 40%, 17~/o, respectively; euhaline > mesohaline-polyhaline > oligohaline for the preservable, 2=42%, 15%, 3%, respectively). The proportion of species collected per sampling that were nonpreservable (2= 54~/o) was significantly greater than the proportion that were preservable (2= 3%) at the oligohaline sites (Duncan's multiple range, ~ = 0.05) but, on the average, these sites had few preservable taxa. The proportions of all taxa collected per sampling that were preservable or unpreservable were not significantly different in either the euhaline or mesohaline-polyhaline sites (Duncan's multiple range, ~ = 0.05). The cumulative species richness of many mesohaline and polyhaline estuarine sites was as high as the continental shelf when considered over a time span of more than 2 yr (Table II), but, as the above analysis indicates, species richness at any one time was usually much less. Hence, the increase in cumulative species richness was produced not by a speciesrich community, but by frequent temporal changes in the community. In contrast, contemporaneous species accounted for much more of the cumulative species richness of the continental shelf. Powell and Stanton (1985) and Staff et al. (1986) stressed the danger of using ecologic

85 theory directly in paleoecology without correcting for time averaging and taphonomy. The relationship of species richness to environmental variability offers a good example. High species richness in death assemblages can just as easily result from environmental variability as from environmental stability. Consequently, the classic relationship between species richness and environmental variability should be used with caution in paleoecology. We add two caveats. (1) Few data are available for the continental shelf. (2) The data are from a variety of sites; no long-term data for a complete estuarine-shelf transect were available. Consequently, additional data would be useful to confirm these predictions,

Persistence of the preservable component The cumulative number of species encountered was plotted against time for each of the long-term data sets, examples of which are presented in Figures 1-11. New species can be encountered in recurrent sampling programs for two reasons: rare species are finally collected or new species are recruited to the sampled area. The former is essentially the problem of sampling ever larger areas at a single time to collect all species present in a community. Such a process can be approximated by a rectangular hyperbolic function relating cumulative species number to sample size (De Caprariis, 1984), thereby estimating a theoretical value for true species richness from incomplete sampling. To determine whether such a technique can be used to estimate a theoretical value for time-averaged species richness in the death assemblage, we used the equation

Y= ax/(1 + bx) where a and b are regression parameters, x is the sample size and Y is the number of species (De Caprariis, 1984). The ratio a/b provides a measure of true species richness at large values of x. Predicted values of cumulative species richness frequently were poor estimates of mea-

sured species richness. Examination of the cumulative curves (e.g. Figures 3 and 4) shows that many were s-shaped, unlike typical cumulative species-area curves. The rate at which new species were encountered was slow initially, then increased rapidly for a time before decreasing in a more asymptotic fashion. The initial s-shape was probably produced by the first large seasonal addition of taxa during the sampling program. We compared the remainder of the curve, subsequent to this first seasonal addition, to the same theoretical model. In 17% of the sites, predicted values of species richness still differed by more than 25% from the observed values. These discrepancies were produced by additional, less extreme sshaped sections in the time series; that is, by relatively short periods where relatively many new species were encountered. Clearly, in these data sets, most new species were encountered as temporal additions or replacements, not the fortuitous sampling of spatially rare taxa. Moreover, extrapolation of values of cumulative species richness to time periods longer than the sampling program, for comparison to the actual species richness of the timeaveraged death assemblage, is not likely to be accurate. No alternative exists to even longerterm sampling programs. Boesch and Rosenberg (1981)define persistence as "constancy in the community over time, irrespective of perturbations". Persistent species remain components of the community for longer periods of time than other species. Temporal replacement is lower either because environmental variability is low or because the physiological limits of the species are relatively broad. The latter two properties are typically inversely proportional. Species richness of the death assemblage is a measure of cumulative species richness in the community over the time during which the entire death assemblage was formed because essentially all preservable species are actually preserved. That is, in spite of the loss of most individuals by various taphonomic processes, at least a few individuals of nearly every species are eventually preserved (Cummins et al., 1986a; Staff

86

et al., 1986). Time averaging perforce incorporates a range of environmental change. The persistence of the preservable component will then determine how the species richness of the death assemblage compares to that of the entire community over this range of environmental change. Thus, is the preservable component more or less persistent than the nonpreservable component of the community? Two cumulative species richness curves, one for the nonpreservable component of the living community and one for the preservable component, were constructed for each site from the long-term data sets in Table II. Each sampling interval on each curve was compared with the immediately preceding one and the proportional increase in the cumulative number of species calculated for each pair (Xt/X~+ 1, where X t is the cumulative number of species collected at time t). If the preservable component was the more persistent, then proportionately fewer new species would be found per sampling interval. Therefore, the proportional increase in the cumulative number of preservable species collected from one sampling to the next would, on the average, be lower than the proportional increase in the nonpreservable component from the same site. The two proportions, for the preservable taxa and nonpreservable taxa, were compared for each pair of sampling intervals and the number of interval pairs where one was larger than the other tallied. The final totals for the site were the number of times that either the proportional increase for the preservable component or the nonpreservable component was higher. These totals were taken as a measure of how the persistence of the nonpreservable and preservable components compared over the entire study, Usually, the curves for the preservable component were flatter than for the nonpreservable component. That is, the rate of species increase appeared slower in the preservable component at the majority of the sites (e.g. Figs.3 and 9). The rate of increase was, in fact, slower on the average. In four (6.0%) of the cases, the two rates of species increase were

equal. Of the remaining 62 sites, only in 15 (24.2%) was the average rate of species increase greater in the preservable component. In the remainder, additional nonpreservable species were encountered at a more rapid rate. This difference, 15 vs. 47, is significantly different from a 50:50 split (binomial test, P < 0.0001). Only in the mid-Atlantic continental shelf and Mediterranean data sets did the ratio, between those cases in which persistence was greater in the preservable component or the nonpreservable component (10:7), not differ significantly from a 50:50 split (binomial test, P=0.12). Hence, the preservable component was significantly more persistent in the lower salinity bays where environmental variability was higher (37 of 45 cases). In the euhaline, environmentally less variable sites, the frequency was not significantly greater than expected by chance even though the preservable component was more persistent at over half the sites (10 vs. 7). On the average, then, the most persistent component of the community is preserved. This is particularly true of environmentally variable h a b i t a t s w h e r e t h e p r e s e r v a b l e c o m p o n e n t must, on the average, have greater physiological tolerances. To this extent, then, the influence of time averaging is minimized. Conclusions Conclusions drawn by comparing studies such as these, from greatly differing geographic areas and employing greatly differing sampling durations, stations and methods, must be used with care. The relationships observed from such comparisons need to be verified with field studies employing similar methods from within similar regions. More long-term studies are needed to establish species richness trends of preservable and nonpreservable benthic assemblages against which fossil assemblages from similar environments can be compared. Nevertheless, analysis of presently available data sets can be used to identify important trends. Only the species richness component of

87 d i v e r s i t y in a d e a t h a s s e m b l a g e or fossil a s s e m b l a g e c o n t a i n s a n y i n f o r m a t i o n on t h e o r i g i n a l d i v e r s i t y of t h e living c o m m u n i t y , b u t e v e n h e r e t h e i n f o r m a t i o n is b i a s e d in s e v e r a l ways. On t h e a v e r a g e , t h e p r e s e r v a b l e species a r e m o r e p e r s i s t e n t t h a n t h o s e species l a c k i n g p r e s e r v a b l e h a r d p a r t s . H e n c e , t h e effect of t i m e a v e r a g i n g s h o u l d be m i n i m i z e d b e c a u s e the p r e s e r v a b l e species will, on t h e a v e r a g e , be p r e s e n t m o r e o f t e n o v e r a l o n g e r period of t i m e t h a n o t h e r species living in t h e s a m e h a b i t a t , Unfortunately, increased persistence cannot offset t h e i m p a c t of the a c c u m u l a t i o n of n o n c o n t e m p o r a n e o u s t a x a . As e n v i r o n m e n t a l v a r i a b i l i t y i n c r e a s e s , species r i c h n e s s in t h e d e a t h a s s e m b l a g e also i n c r e a s e s (given s i m i l a r s e d i m e n t a t i o n rates). T h i s is p a r t i c u l a r l y t r u e in m e s o h a l i n e a n d p o l y h a l i n e h a b i t a t s w h e r e t h e r e l a t i v e l y g r e a t e r p e r s i s t e n c e of t h e pres e r v a b l e c o m p o n e n t c a n n o t offset the effects of e n v i r o n m e n t a l v a r i a b i l i t y . C o n s e q u e n t l y , the w e l l - k n o w n e c o l o g i c a l r e l a t i o n s h i p of decreasing species r i c h n e s s w i t h i n c r e a s i n g e n v i r o n m e n t a l v a r i a b i l i t y m a y be p o o r l y p r e s e r v e d . An i m p o r t a n t question, then, is: c a n a species-rich a s s e m b l a g e f o r m e d by t i m e a v e r a g ing of n o n c o n t e m p o r a n e o u s t a x a living in a v a r i a b l e e n v i r o n m e n t be d i s t i n g u i s h e d f r o m a species-rich a s s e m b l a g e f r o m a d i v e r s e c o m m u n i t y in a less v a r i a b l e e n v i r o n m e n t ? We s u g g e s t t h a t c e r t a i n a s p e c t s o f the sizef r e q u e n c y d i s t r i b u t i o n s of t h e t a x a m i g h t p r o v e useful, p a r t i c u l a r l y the n u m b e r of t a x a w i t h adults, t h e n u m b e r of t a x a w i t h m a n y indiv i d u a l s r e a c h i n g m a x i m u m size, a n d t h e humber of i n d i v i d u a l s of t a x a h a v i n g a l o n g life span. E a c h of t h e s e is a m e a s u r e of p e r s i s t e n c e in t h e c o m m u n i t y a n d e a c h r e q u i r e s a relatively stable e n v i r o n m e n t a l r e g i m e for considerable periods of time. M a n y species re c r u i t i n g to e n v i r o n m e n t a l l y v a r i a b l e h a b i t a t s fail to p r o d u c e a d u l t s or i n d i v i d u a l s of m a x i m u m size ( C u m m i n s et al., 1986b). T a x a living in d i v e r s e c o m m u n i t i e s in s t a b l e e n v i r o n m e n t a l r e g i m e s should produce adults and individuals near m a x i m u m size m u c h m o r e often. W e e m p h a s i z e the i m p o r t a n c e of t e s t i n g this h y p o t h e s i s . T h e i n t e r p r e t a t i o n of species r i c h n e s s as a paleo-

community attribute with real ecological m e a n i n g will r e q u i r e d a t a b e y o n d simply t h e n u m b e r of species in t h e fossil a s s e m b l a g e . T a p h o n o m y a n d t i m e a v e r a g i n g do n o t p e r m i t a c l e a r i n t e r p r e t a t i o n of j u s t t h a t d a t u m . Acknowledgements W e t h a n k A. F. H o l l a n d , D. F. Boesch, R. J. Diaz a n d the T e x a s W a t e r D e v e l o p m e n t B o a r d for m a k i n g t h e i r d a t a a v a i l a b l e to us. J. Parr a c k offered s u g g e s t i o n s t h a t i m p r o v e d the m a n u s c r i p t . R. C o v i n g t o n t y p e d the m a n u s c r i p t a n d tables. T h i s r e s e a r c h w a s funded by t h e N a t i o n a l S c i e n c e F o u n d a t i o n g r a n t Nos. EAR-8302339 a n d EAR-8506043. We a p p r e c i a t e this s u p p o r t .

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