Field and laboratory experiments on interactions ... - Science Direct

J. Exp. Mar. Biol. EC&. , 168 (1993) 259-278 0 1993 Elsevier Science Publishers B.V. All rights reserved

JEMBE

259 0022-0981/93/$06.00

01954

Field and laboratory experiments on interactions among an infaunal polychaete, Nereis diversicolor, and two amphipods, Corophium volutator& C. arenarium: effects on survival, recruitment and migration K. Thomas Jensen a and Carl Andrbb “fnstituce oj*Biological Sciences, Department ofEcok~gy and Genetics, University of&rhus, Denmark; b Department of Zoology. Stockholm University, Stockholm, Sweden (Received

14 January

1992; revision

received

8 December

1992; accepted

21 January

Aarhus,

1993)

Abstract: The purpose of this study was to examine if a soft-bottom polychaete (Nereis diversicolor) affected two congeneric amphipods (Corophium volutator and C. arenarium) differentially and thereby contributed to their co-occurrence on intertidal mudflats. The influence of N. diverscolor on the two Corophium species was studied in field and laboratory experiments. Neither of the experiments corroborated earlier findings of N. diversicoior as an important predator on C. volutator. However, enclosed populations of C. arenarium exhibited enhanced mortality in the presence of N. diversicolor. In short-term laboratory experiments N. divers&z&r caused an increased migration rate in both Coro~hi~ species. Recruitment patterns of N. diversicofor and Corophium during the field experiment suggest that high densities of juvenile N. diver~~colorimpair the recruitment of Corophium. Although the actual mechanisms causing these varied effects of Nereis diversicoior on the two Corophium species are largely unknown, some evidence suggest that under field conditions N. diversicolor alters the substratum by its mucuous production, and thereby creates a more silty environment which favors C. YOlutator but not C. arenarium. Under the present laboratory conditions, where suspension feeding in N. dive&color was an insufficient method to provide food, disturbance caused by surface active N. diversicolor specimens is a likely explanation of the negative impact of N. diversicolor on both Corophium species. In conclusion, the effects that N. diversicolor might have on co-occurring species is probably dependent on its choice of feeding method, which in turn is supposed to be a result of the availability of food both on the bottom and in the water. Distributional consequences for the Corophium species of these interactions are discussed. Key words: Amphipods;

Competitor;

Enclosure;

Polychaete;

Predation;

Recruitment

INTRODUCTION

To understand processes causing distributional patterns of marine species is an important goal to marine ecologists. Most intriguing and the subject of several studies has been spatial patterns among congeners (or guild members) from near-coastal soft-bottom habitats (estuaries, intertidal mudflats) (Muus, 1967; Fenchel, 1975; Correspondence address: K.T. Jensen, Institute of Biological Sciences, Genetics, University of Aarhus, Building 540, Ny Munkegade, 8000 Aarhus

Department C, Denmark.

of Ecology

and

260

K.T. JENSEN AND C. ANDRi?

Fenchel & Kolding, 1979; Cherrill & James, 1987; Kristensen, 1988; Jensen & Kristensen,

1985; Hylleberg, 1986; Hill & Elmgren, 1990). Preadaptation to certain sets of

environmental variables (salinity, substratum, exposure etc.) and spatial heterogeneity may explain why each guild member has a peak occurrence at certain combinations of variables (Connell, 1980). However, the realized niche of each guild member is less than their fundamental niche, and in accordance with “the competitive exclusion principle” this has often been interpreted as a result of interspecific competition. Depending on the environmental settings a species may be either competitively superior or inferior compared to a congener. However, unless some kind of territoriality or interspecific aggression is involved, competitive exclusion of an inferior species from the micro/macro-habitat of a superior species appears to be a rather unusual event (Peterson, 1979; den Boer, 1986; Gallagher et al., 1990). Often, other biotic processes like predation and parasitism, reduce the significance of interspecific competition by acting selectively on a superior competitor (den Boer, 1986; Holmes & Price, 1986; Minchella & Scott, 1991). Such processes could also cause spatial segregation among competitors as suggested from some studies (Hill & Elmgren, 1987; Jensen & Kristensen, 1990). The purpose of the present study was to examine whether a soft-bottom infaunal polychaete (Nereis diversicolor O.F. Milller) could contribute to the co-existence of two infaunal amphipods [ Corophium volututor (Pallas) and C. arenarium Crawford]. Some laboratory studies suggest that N. diversicolor may be an important factor controlling the abundance of C. volutator, either through predation (Rdnn et al., 1988) or disturbance (olafsson & Persson, 1986). C. volututor and C. arenarium are sympatric on some intertidal mudflats and both Corophium species inhabit U-shaped burrows in the upper 5-10 cm sediment layer (Jensen & Kristensen, 1990). Frequently, N. diversicolor cooccurs with the two Corophium species on intertidal mudflats. A priori we would expect that both species due to their ecological similarity would show the same negative response to the presence of N. diversicolor. However, the occurrence of dense populations of both N. diversicolor and C. volutator at some localities (estuaries and lagoons) (Michaelis, 1981; Jensen, 1988) does not support a strong negative interaction among these two species. Realizing that N. diversicolor that are inundated permanently may exhibit behaviour different from individuals subjected to a tidal cycle (another regime of predators and food), we conducted experiments at two sites. To assess the possible impact of N. diversicolor on the Corophium species and the mechanisms involved we performed field and laboratory experiments. In the field experiment WC examined: (1) if N. diversicolor enclosed with either of the two Corophium species affected them differentially, and (2) whether the impact of adult N. diversicolor on C. volututor differed between localities (intertidal mudflats versus subtidal mud-bottoms). To determine to what extent predation or interference interactions (competition, disturbance) was the underlying mechanisms causing possible effects of N. diversicolor on Corophium species, we conducted short-term laboratory experiments that allowed us to assess the relative importance of the two possible mechanisms.

INTERACTIONSAMONGNEREIS AND COROPHIUM

SPECIES

261

MATERIALS AND METHODS STUDY SITES The field experiments were conducted on an intertidal mudflat and in a saltwater lagoon both situated in the southern part of the Danish Wadden Sea (54”56’ N, 8’ 39’ E). Characteristics of the areas have been reported previously (Jensen, 1988; Jensen & Kristensen, 1990). The lagoon is not subjected to a tidal shift between emersion and submersion as is the intertidal flat. However, being a shallow water basin (depths to z 50 cm) parts of the bottom occasionally become emersed due to wind driven movements of the water body. CAGING EXPERIMENTS Each cage consisted of a PVC core (base) with a diameter of 8 cm and a length of 30 cm onto which a detachable 10 cm high top made of 1 mm mesh was screwed. The bases of the cages were pushed into the mud until z 1 cm was exposed above the sediment surface. Sediment enclosed by the cores was removed and the cores were refilled with sediment that had been sieved through a 500 pm sieve to remove the macrofauna. Two experiments were done to study the effect of adult N. diversicolor on survival and recruitment of Corophium species. One was conducted on a intertidal mudflat (FLAT-exp.) and the other in a shallow saltwater lagoon (LAGOON-exp.). FLAT-experiment: On the mudflat a total of 36 cages were used. These contained the following nine treatments (C.V.: C. volutator; C.a.: C. arenarium; N.d.: N. diversicolor): (1) no animals; (2) 5 N.d.; (3) 10 N.d.; (4) 5 N.d. + 30 C.V.; (5) 10 N.d. + 30 C.V.; (6) 5 N.d. + 30 C.a.; (7) 10 N.d. + 30 C.a.; (8) 30 C.V.; (9) 30 C.a.; each replicated in four cages. Each cage was positioned randomly within a x 50 m2 grid (1 m between cages) located ~400 m from the mean highwater line. This experiment was carried out from 13 May to 9 June, 1988 (27 days). LAGOON-experiment: A total of 30 cages were used. These contained the following six treatments: (1) no animals; (2) 5 N.d.; (3) 10 N.d.; (4) 30 C.V.; (5) 57 N.d. + 30 C.V.; (6) 10 N.d. + 30 C.V., each replicated in five cages. Each cage was positioned randomly within a = 30 m2 grid (1 m between cages). This experiment was done from 12 June until 5 August, 1986 (54 days). The densities used are within the range of adult densities: 5 and 10 N. diversicolor cage -’ correspond to 1000 and 2000 individuals.mm2, respectively, and 30 Corophium individualsecage-’ corresponds to 6000 individuals.m-2. Smaller individuals of N. diversicoZorwere used in the 10 N.d. treatments compared to the 5 N.d. treatments to avoid artificial size-density combinations. Mean body lengths (formaldehyde preserved specimens) of small and large N. diversicolor used in the experiment were 42.2 mm (k 12.2, SD) and 68.0 mm ( + 6.8, SD), respectively. The numbers of adult Corophium are below peak numbers of adults (S-10000 individuals*m-2), but as such numbers

262

K.-T. JENSEN

AND C. ANDR6

are seldom maintained for long periods, we chased a lower density for our experiments. In addition, we wanted to avoid density dependent behaviour of Corophium influencing consumption by N. diversicolor. Specimens of Corophium and Nereis were collected at the study sites (mudflat and lagoon). Individuals of Corophj~~nwere identified under a dissecting microscope and each species was kept in separate aquaria. I~di~du~s for the various treatments were picked at random from these aquaria and brought to the field in separate jars. All handling of live animals was done with soft tweezers to avoid injury to the animals. Corophiumindividuals were allowed to establish within cages before N. diversicolorwere added. At the end of the experiments the content of each cage was sieved and all animals retained on a 500 pm sieve. The samples were preserved in 40.0 buffered formaIdehyde. Individuals of ~oro~hj~rnwere measured from the anterior margin of the rostrum to the posterior margin of telson ( 12 x magnification). They were identified to species when > 2 mm and to sex when > 3.3 mm. Individuals of :V. divetxicolor from both experiments were measured to nearest mm. To determine food items selected by N. diversicolor all individuals from 5 N.d.addition treatments in 1988 were dissected and their stomach contents examined.

LABORATORY

EXPERIMENTS

Five days before each experiment specimens of N. diversicolor, C. volututor, C. arenarium and sediment (fine sand) were collected from the study area. The animals were transferred to our laboratory at Rsnbjerg (Limfjorden), and kept in tanks with running seawater. Two experiments were performed, Exp. 1 in May and Exp. 2 in November 1988, following the same design. In the experiment we used flow-through circular plastic aquaria, (105 mm high by 100 mm inside diameter), tilled with sediment, sieved through a 0.5 m mesh, to a depth of 60 mm. The aquaria were divided in two compartments by a net (1 mm mesh size), which extended 20 mm above the sediment surface. The net should prevent N. diver.sicolor from moving from one compartment to another, but allow C. volutator and C. arenarium to migrate via the 25 mm deep water column. Zero (controls), one large or tree small N. diversicolor were placed in one compartment and were allowed to establish themselves. After 4 h we added 20 individuals of C. vnlutator or C. arenarium to the N. diversic~~~r-~omp~tments. They were allowed to establish before water was led to the aquaria. The densities correspond to 0,250 and 750 N. diversicolor and 5000 Corophium m -2. The body lengths of specimens (alcohol preserved; mean + SD; in mm) used in the experiments were for C. voiutator7.7 + 1.1 (May) and 7.0 t_ 1.O (November); for C. arenurium 5.6 i: 0.6 (May) and 5.2 rf:0.6 (November); for small N. diversicolor 36.6 rf~9.7 (May) and 33.1 k 6.3 (November); for large N. diversicolor 64.6 + 4.2 (May) and 56.3 f 10.1 (November). During the experiments the water-flow was ‘=:20 mlemin -I, salinity 277&, S, and temperature 17 “C (Exp. 1) and 14 “C (Exp. 2): the experiments were run under natural day/night light regime.

INTERACTIONS

AMONG

NEREZS

AND

COROPHZUM

SPECIES

263

In the first experiment (May, 1988), there was a high mortality of both Corophium species, regardless of experimental treatment. Therefore, we repeated the experiment in November 1988. At that time, however, C. arenarium had become scarce on the mudflat and we excluded the treatment C. arenarium + 3 N. diversicolor, and cut down the number of replicates to four for the remaining treatments with C. arenarium. In all other treatments there were five replicates. The location of each aquarium and compartment was randomized. After 5 (Exp. 1) or 6 (Exp. 2) days the sediment and animals from each compartment were washed through a 0.5 mm screen. The Corophium individuals from each compartment were then counted, measured and sexed. Migration rates are calculated as the percentage of the total number of surviving individuals, that were found in the non-addition compartment.

STATISTICAL

ANALYSES

Differences between treatments in survival rates of Corophium and abundances of recruits (field experiments), and emigration and survival rates (lab. experiments) were analysed for significance by analyses of variance using SPSS (Hull and Nie, 1981). If data did not met the assumption of homogeneity of variances (according to Cochrans test) they were transformed to ln(x + l), which stabilized the variances in all cases. Analyses of unbalanced designs were solved by ordering each term last in the design, i.e. each term is corrected for every other term in the model (UNIQUE-procedure, Hull and Nie, 1981). Tukey’s test (with Kramers modification in case of unbalanced data) was used to compare individual treatments (Day and Quinn, 1989).

RESULTS

Ambient fauna Faunal compositions at the end of the experiments on the extant bottoms near the experimental plots are shown in Table I. The mudflat fauna consists of typical representatives of the “Macoma balthica” community. At the experimental site the fauna was strongly dominated by juveniles of C. volutator,M. balthica, Pygospio elegans, Polydora ligni and N. diversicolor in June 1988. Both Corophium species co-occurred in low numbers near the experimental plot in this period. Usually the lagoon fauna is dominated strongly by C. volutator and N. diversicolor, as it was in August 1986. These two species may reach maximum numbers of 53000 ind:me2 and 6000 ind:mp2 (Jensen, 1988), respectively, and in general they constitute more than 90% of all individuals. The following species would be expected to colonize the mudflat enclosures as assessed from the presence of juveniles on the extant bottom: C. volutator, C. arenarium, A4. balthica, P. elegans, P. ligni and N. diversicolor, while only C. volutator and N. diversicolor are possible immigrants to the lagoon enclosures. Only recruits of the two latter species plus C. arenarium recruits will be treated in this paper.

K.T. JENSEN

764

AND C. ANDRE

TABLE

Species composition

I

near the experimental plots at the mudflat (9 June, 1988; n = 6) and in the lagoon (7 August, 1986, n = 10). Mean numbers 50 cm- ’ k SE. FLAT

Species Oligochaeta Tuhificoides benedeni Polychaeta Capiteila capitata Heteromastus filiformis Nereis dive&color (all) adults juveniles ( < 2 cm) Pygoospioeiegans Po!vdora ligni Gastropoda Hydrobia ulvae Bivalvia Macoma balthica Mya arenaria Crustacea Corophium arenarium adults juveniles (< 3.3 mm) Corophium volutator adults juveniles (< 3.3 mm) * No standard error is indicated were measured.

as specimens

LAGOON

20.33 2 4.1

0.00

0.67 + 0. I 6.17k2.0 9.00&4.1 0.00 9.00 + 4.1 56.17 f 12.0 17.67 f 3.Y

0.00 0.00 22.90 * 1.2 7.60* 19.50* I .60f 0.9 0.00

13.60 i 3.4

0.30 + 0.2

29.61 at8.3 1.17~0.6

0.00 0.00

15.67 5 4.0 10.00 + 3.0 5.67 f 1.7 91.17 2 19.8 14.83 it_5.6 77.50+ 16.1

0.00

picked from individual

114.00 f 13.3 43.66* 70.34* samples had been pooled before they

Survivorship of enclosed individuals of N. diversicolor

The survival of N. diversicolor was higher during the FLAT-exp. than during the LAGOON-exp., but at the end of both experimental periods high numbers of adult N. diversicolor still persisted (Table II). The difference in numbers of survived specimens could be a result of the shorter duration of the FLAT-exp. compared with the LAGOON-exp. Escape through the bottom of the cages or mortality of enclosed individuals are both possible causes of the reduction in numbers of N. diversicolor individuals. Influence of N. diversicolor on enclosed populations of Corophium

We designed the FLAT-exp. to test if N. diversicolor affected adult individuals of the two congeneric species C. volutator and C. arenarium differentially. C. arenarium showed a higher survival rate within control treatments than C. volututor (32.50/, versus 5.0%, Fig. 1). This pattern changed when each Corophium species was enclosed together with N. diversicolor. The interaction among the two factors (Nereis density and

INTERACTIONS

AMONG NEREIS AND COROPHIUM

SPECIES

265

TABLE II Mean survival of adult N. diversicolor (numbercage - 1 and percentage survived) in the experimental treatments on the mudflat (FLAT-exp., 13 May to 9 June 1988, 27 days) and within the Saltwater lagoon (LAGOON-exp., 12 June to 5 August 1986, 54 days). N.d. = N. diversicolor; C.V. = Corophium volutator; C.a. = C. arenarium. Experimental Site

Treatment

5 N.d. 10 N.d. 5 N.d. 10 N.d. 5 N.d. 10 N.d.

+ 30 C.V. + 30 C.V. + 30 C.a. + 30 C.a.

FLAT

LAGOON

4.0 (80.0%) 8.3 (83.3%) 4.8 (95.0%) 8.3 (83.3%) 4.8 (95.0%) 8.3 (82.5%)

2.8 (55.0%) 4.0 (40.0; 0.05). The sum of squares and degrees of freedom (df) associated with the residual sum of squares and df. Recruits

of

Effect of experimental site

c. ~t~luturora

Effect of Nereis density (O/5/10)

df 1 Mean square 16.73 51.71*** F -_______------------------_-----------------

!V. diver.sicobr

df Mean square F

Effect of Corophium density (O/30)

2 O.% I .70”-‘-

1

1

23181.43 1s3.37***

583.08 4.61*

lagoon), N. ~jve~~~~~o~dennumbers of C. ~~~~rur~~and interaction effects were not with these effects are pooled

1 3.16 9.77**

I 2 I .03 0.17”’

Residual (error) 46 0.32

46 126.42

n.s.: non-significant. +pc0.05; **pt0.01: ***p