253 (2000) 33–48
www.elsevier.nl / locate / jembe
Epibenthic amphipod abundance and predation efficiency of
the pink shrimp Farfantepenaeus duorarum (Burkenroad,
1939) in habitats with different physical complexity in a
tropical estuarine system
a ,* a b
´ Adriana Corona , Luis A. Soto , Alberto J. Sanchez
a
´ ´
Laboratorio de Ecologıa del Bentos, Instituto de Ciencias del Mar y Limnologıa,
´ ´
Universidad Nacional Autonoma de Mexico, Ciudad Universitaria, Circuito exterior s /n, A.P. 70-305,
´ ´
Mexico04510, D.F., Mexico
b
´ ´ ´ ´
Laboratorio de Hidrobiologıa, Division Academica de Ciencias Biologicas,
´ ´ ´ ´
Universidad Juarez Autonoma de Tabasco, Km 0.5 Carretera Villahermosa-Cardenas, Tabasco, Mexico
Received 23 February 1999; received in revised form 31 May 2000; accepted 6 June 2000
Abstract
Amphipod abundance and biomass were determined in soft-bottom substrates (SBS), mono-specific Thalassia testudinum patches and T. testudinum with attached macroalgae (SAV) from
´
Terminos Lagoon. Amphipods were absent in SBS, and their density and biomass were higher in
22 22 22
SAV (3351 individuals m , 1718 mg AFDW m ) than in T. testudinum (1220 ind m , 625 mg
22
AFDW m ). Although macroalgae and seagrasses are recognised as an alternative refuge against predation for amphipods, the high abundance of amphipods in SAV suggests that macroalgae represent a habitat that provides greater food availability. Pink shrimp Farfantepenaeus duorarum (Burkenroad, 1939) consumption rate (Mo) of epibenthic amphipods was experimentally
evalu-21
ated. Mo intensifies as prey density increases and varied from 0.39 to 2.39 mg AFDW h . Predation efficiency of F. duorarum on epibenthic amphipods was also evaluated in four artificial habitats with different physical complexity: soft-bottom substrates (SBS), small woody debris
22
(SWD), seagrasses with densities of 300 and 1200 shoots m (S300 and S1200, respectively),
22
macroalgae (MA), and at two prey densities (962 and 2406 ind m ). Amphipod consumption rate
21
by F. duorarum varied from 1.20 to 2.07 ind h in S1200 and MA, respectively. Habitat complexity had a significant effect on consumption rate, but prey density did not. Habitat physical complexity and predation efficiency maintained an inverse and a non-linear relationship. Presumably, the decrease in predation efficiency in association with the habitat complexity is due to the differential refuge value of these habitats. However, predation efficiency may also be influenced by either the microhabitat use by amphipods, the shrimp’s dependence on seagrasses, or
*Corresponding author. Tel.: 152-6-225-835; fax: 152-6-160-748.
E-mail addresses: [email protected] (A. Corona), [email protected] (A.J. ´
Sanchez).
by differences in habitat value caused by the diel behavioural distribution pattern of amphipods and shrimp. Both field and experimental results highlight the importance of evaluating the relative value of tropical estuarine habitats through the study of the relationship between habitat physical complexity and predator–prey interactions. They also emphasise that inherent biological and ethological factors of the predator and prey involved, coupled to spatial and temporal variations in the habitat, should also be considered. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Farfantepenaeus duorarum; Predation efficiency; Habitat complexity; Amphipods; Mexico
1. Introduction
Estuarine ecosystems are characterised by high habitat heterogeneity which is a result of the spatial arrangement of seagrasses, macroalgae, soft-bottom substrates, hard substrates and small woody debris (Leber, 1985; Heck and Crowder, 1991; Everett and Ruiz, 1993). Estuarine heterogeneity may be responsible for their high productivity and for the differential distribution, abundance and species richness of associated fauna (Young and Young, 1978; Leber, 1985; Russo, 1987; McCoy and Bell, 1991). The high variability in species abundance and diversity recorded among estuarine habitats has been attributed to the relative value of the component habitats, to their temporal variation and to their spatial arrangement (Stoner, 1980; Heck and Thoman, 1984; Orth et al., 1984). Usually, decapods and peracarid crustaceans are abundant in estuaries. The former group includes species of commercial value like the pink shrimp,
Farfan-tepenaeus duorarum, that dominates the associated fauna of estuarine macrophytes
(Gore et al., 1981; Leber, 1985; Minello and Zimmerman, 1991) and is an opportunistic omnivorous predator on polychaetes, molluscs, macrocrustaceans, fish and detritus (Nelson, 1981; Leber, 1985; Nelson and Capone, 1990; Pattillo et al., 1997). Among the peracarids, the amphipods high abundance, species diversity and feeding habits make them of potential nutritional value to some ontogenetic phases of estuarine tropical predators (Bierbaum, 1979; Zimmerman et al., 1979; Price and Hylleberg, 1982; Poovachiranon et al., 1986; Minello and Zimmerman, 1991). Amphipods represent food items normally consumed by pink shrimp (Nelson, 1979a, 1981).
Predation and habitat physical complexity interaction are two of the main factors that affect the biotic structure of estuarine coastal systems. Habitat physical complexity is a function of the number of microhabitats or refuges available to the associated fauna and has differential value for invertebrate populations as refuge or feeding sites (Stoner and Lewis, 1985; McCoy and Bell, 1991). Habitat relative value is defined by the increase in prey survival and food availability (Coen et al., 1981; Minello and Zimmerman, 1991; Kenyon et al., 1997). Although estuarine heterogeneity is widely recognised, in most studies in which habitat relative value has been assessed, only the physical complexity of some of all habitats present in a system has been considered (Ware, 1972; Bierbaum, 1979; Coen et al., 1981; Crowder and Cooper, 1982; Heck and Thoman, 1984; Holmlund et al., 1990; Sheridan, 1992; Everett and Ruiz, 1993).
shrimp Penaeus aztecus, for instance, reduces amphipod abundance with efficiencies higher than 90% (Nelson, 1979b), and similar values have been also recorded for P.
duorarum on seagrass macrofauna (Nelson, 1981). A positive relationship between
increase in prey survival and higher habitat physical complexity in seagrass patches, macroalgae, soft-bottom substrates or woody debris has been described for macrofaunal organisms (Crowder and Cooper, 1982; Wilson et al., 1990; Sheridan, 1992; Everett and Ruiz, 1993; Dittel et al., 1996). This relationship was recorded for the pink shrimp P.
duorarum preying upon polychaetes in soft-bottom substrates and epifauna of seagrass
beds (Nelson, 1981; Leber, 1985; Nelson and Capone, 1990). However, few studies have compared the relationship between a predator–prey system and the habitat physical complexity for shrimp predators and for a greater variety of habitats. The objectives of this study are to assess the effect of habitat physical complexity on amphipod distribution and the predator–prey interaction between Farfantepenaeus duorarum and
´
gammarid amphipods in Terminos Lagoon, a tropical estuarine system in southeastern ´
Mexico.
2. Materials and methods
2.1. Study area
The study area is a shoal known as ‘El Cayo’ located in the inner margin of ‘El
´ ´
Carmen’ barrier island of Terminos Lagoon in the Gulf of Mexico (Fig. 1). Habitats at ‘El Cayo’ include soft-bottom substrates, mangrove woody debris and broad meadows of
¨ submerged aquatic vegetation dominated by Thalassia testudinum Banks ex Konig,
¨
Halodule wrightii Aschers, Syringodium filiforme Kutz, red (Lawrencia spp., Gracilaria
spp., Hypnea spp. and Acanthophora spp.), green (Caulerpa spp.) and brown (Dictyota
´ ´
spp.) macroalgae (Raz-Guzman and De la Lanza, 1991; Sanchez, 1997). The area has high crustacean abundance and diversity and serves as a nursery ground for immature
´ ´
stages of penaeid shrimp (Sanchez and Raz-Guzman, 1997).
2.2. Habitat selection
At ‘El Cayo’ we selected habitats that best represented the most extensive heteroge-´
neous habitats of Terminos Lagoon: sandy soft-bottom substrates (SBS), small woody debris from mangrove trees (SWD), monospecific Thalassia testudinum beds and patches of macroalgae (Lawrencia spp. and Champia spp.) attached to T. testudinum (SAV). Their differential architectural complexity suggests that they may have different relative value as habitat for dominant fauna components such as amphipods.
2.3. Amphipod species composition and abundance
Epibenthic core samples were collected in SBS, monospecific T. testudinum patches ´
´
Fig. 1. Study area at Terminos Lagoon in the southeast of Mexico.
1985; Costello and Myers, 1996), five core samples were taken in each habitat during
22
one day in July 1996. A sediment core of 0.05 m was modified with two sharp blades attached at the lower end to sample the standing stock of aquatic vegetation. Samples were sieved through a 0.5 mm mesh and fixed in 10% formaldehyde. Organisms were sorted and transferred to 70% ethylene alcohol. The taxonomic criteria of Bousfield (1973) and Ledoyer (1986) were used to identify amphipods to species level. The epibenthic guild of amphipods was defined according to the microhabitat use of species reported by Nelson (1979a,b) and Stoner and Lewis (1985).
Prey treatments in experimental sections were defined using both abundance (total
22
number of individuals collected) and density (ind m ) estimates in each sample. Their
22 biomass was measured and expressed as ash-free dry weight (AFDW) per m according to an amphipod weight constant of 0.513 mg AFDW proposed by Corona (1998).
Amphipod density and biomass were evaluated with respect to the qualitative and quantitative physical complexity of the three habitats. Qualitative complexity is determined by the physical structure of the substrate and is evaluated as the number of substrates and their architecture (Edgar, 1983; McCoy and Bell, 1991). Monospecific T.
testudinum patches were considered as having less qualitative physical complexity due
to its simple leaf architectural structure, while SAV attain a much higher complexity since other macroalgae (Lawrencia spp. and Champia spp.) are attached to the T.
substrate biomass (Heck and Wetstone, 1977; Virnstein et al., 1984; Leber, 1985) and
22
expressed in mg AFDW m , as an indicator of standing stock supporting capacity of a given habitat. The core samples dry weight was determined after drying at 806108C for 72 h, and then were burned at 5508C for 1 h. T. testudinum epiphytes were eliminated with 10% HCl for 24 h.
2.4. Predator consumption rate
The consumption rate of Farfantepenaeus duorarum (3.0–17.0 mm cephalothoracic length, CL) on epifaunal amphipod prey was evaluated to define experimental densities in which predator foraging effort would not be masked. Both prey and predators were caught with a Renfro beam trawl (Renfro, 1962) over T. testudinum seagrass patches at ‘El Cayo’ from April to July of 1996. Organisms were acclimated in fiber glass cylindrical containers of 40 and 700 l, where mortality was less than 1%. Shrimps were isolated and starved for 24 h prior to each trial. Seven prey density treatments with 15 replicates were used in the experimental design: 5, 10, 15, 20, 25, 30 and 40 amphipods / aquarium. These prey number represented 481, 963, 1444, 1926, 2407, 2888
22
and 3852 ind m , respectively.
In order to avoid experimental error, every experimental aquaria used was a cylindrical plastic container of 1 l, filled with brackish filtered water from the lagoon,
21
with mean temperature (278C), oxygen (5 ml l ), and salinity (35‰) conditions kept constant throughout the experiment. In each trial, a shrimp and an amphipod prey (at a specific density treatment) were kept in an aquarium devoid of substrate for periods of 3 h. Ten of the 105 trials were run each night from April to June, since the number of aquarium was restricted to ten, and the randomised assignation of prey density and predator depended on availability. Trials were run at night between 1800 and 2200 h, considering the periods of maximum activity of these organisms (Hughes, 1968;
´
Subrahmanyam, 1976; Mier y Reyes et al., 1997; Sanchez, 1997).
Consumption rate (Mo), defined here as the number of amphipods eaten by F.
duorarum in 1 h, was calculated by dividing the 3-h consumption by three. The
differential effects of the prey density treatments on consumption rate was graphically analysed by plotting the median value of each treatment.
2.5. Habitat complexity
The relationship between pink shrimp predation efficiency and habitat physical complexity was experimentally tested using soft-bottom substrates, small woody debris, seagrasses and macroalgae. These habitats were artificially represented assuming differences in their architectural complexity and were simulated with: fine sand which had been previously sterilised at 808C for 2 h as soft-bottom substrates; Rhizophora
mangle logs of 9.8 cm length and 2.6 cm diameter which were kept a few days in
freshwater to eliminate toxic tannin concentration before being used as woody debris; seagrasses at low and high shoot density were simulated with the leaf model of T.
22
testudinum at a density of 300 and 1200 shoots m ; the leaf model of Lawrencia spp.
Experimental conditions were standardised by constructing each shoot of Thalassia with three polyethylene blades of 1.5 cm width and 9 cm length. The frond model of
Lawrencia spp. was simulated by a 3-mm width non-uniform short-branched clump of
polyethylene and the same weight of polyethylene used in the low seagrass density habitat was used in the artificial macroalgae. Every seagrass shoot and macroalgae frond was stapled to an acrylic mesh, which was then covered with the same volume of sterile sand used in soft substrates to eliminate artificial substrate buoyancy. Habitat structural characteristics were kept constant in all trials. Predation on amphipods by F. duorarum was evaluated in these habitats whose physical complexity progressively increased from soft bottoms substrates, woody debris, low seagrass density, macroalgae to high seagrass density.
Shrimps from 6.5 to 7.5 mm CL were chosen due to their frequent occurrence in the study site. The prey population was the epibenthic guild of amphipods. Prey and predator maintenance and experimental conditions were the same as used in Section 2.4. In this experimental design each trial included one shrimp, an amphipod prey density and an artificial substrate, kept in a 1-l cylindrical aquarium. Both the prey density and the habitat type were randomly assigned to each aquarium. Each experimental treatment was replicated ten times, and ten trials out of the 100, were run each day between June and July depending on availability.
The consumption rate (Mo) response was used to define the pink shrimp predation efficiency. Our experimental design was a two-factor factorial design (Montgomery, 1991). The predation efficiency variate was statistically determined through a Poisson generalised log-linear model by applying GLIM 3.77 statistical package (Generalised
22 Linear Interactive Modelling, 1985). The effects of prey density (963 and 2407 ind m ) and habitat physical complexity (SBS, SWD, S300, MA and S1200) factors, with their interaction, were evaluated by sequential hierarchical models. The deviance term was used to define the analysis table (Healy, 1988; Aitkin et al., 1989). The within factor comparisons were made by calculating the 95% confidence intervals for each treatment.
3. Results
3.1. Amphipod species composition and abundance
In the three habitats sampled, gammarid amphipods were only recorded on patches of
T. testudinum and SAV; none were found on soft-bottom substrates. A total of 1120 amphipods from 15 species was identified in both habitats, and included 11 epifaunal species, three infaunal, and one Corophium sp.1, whose microhabitat use could not be defined (Table 1).
In the T. testudinum patches, nine species comprised the epibenthic guild of amphipods. A mean abundance of 60 individuals per core resulted in a mean density of
22 22
1220 ind m and mean biomass of 626 mg AFDW m . Quantitative habitat
complexi-22
Table 1
´
Amphipod specific abundance in habitats with different physical complexity in Terminos Lagoon:
mono-a
specific Thalassia testudinum and T. testudinum with attached macroalgae (SAV) patches
Family / species CORE
Thalassia testudinum SAV Melitidae
Melita nitida Smith, 1873* 2 4
Melita planaterga Kunkel, 1910* 73 49
Melita sp.1* 0 3
Elasmopus levis Smith, 1973* 42 60
Elasmopus sp.1* 7 13
Maera quadrimana (Dana, 1953)* 0 19
Eusiridae
Nasageneia yucatanensis Ledoyer, 1986* 1 0 Amphilochidae
Gitanopsis laguna McKinney, 1978* 28 53
Phoxocephalidae
Paraphoxus spinosus Holmes, 1905** 0 63
Ampeliscidae
Ampelisca vadorum Mills, 1963** 0 3
Aoridae
Grandidierella bonnieroides Stephensen, 1948* 38 4 Ampithoidae
Cymadusa compta (Smith, 1873)* 47 70
Photidae
Gammaropsis togoensis (Schellemberg, 1925)* 61 474 Corophiidae
Cerapus benthophilus Thomas and Heard, 1979** 0 5
Corophium sp.1*** 0 1
Species richness (S ) 9 14
Total abundance 299 821
a
Microhabitat use is indicated as: * epifaunal, ** infaunal, *** not defined. Taxonomic species arrangement according to Bousfield (1973).
In SAV, the guild included ten epifaunal species. Their mean abundance per core and
22
density were 150 individuals and 3057 ind m , respectively. Amphipod biomass in
22 22
SAV was 1567 mg AFDW m . The biomass of SAV was 133 108 AFDW m , and its relationship with amphipod density and biomass was indicative of how many organisms per mg AFDW can this habitat sustain.
Species richness of the guild was similar in both habitats. Amphipod density and biomass were 2.5 times higher in SAV than in T. testudinum. SAV had a greater qualitative physical complexity caused by the leaf architecture of the macroalgae
Lawrencia spp. and Champia spp. attached to T. testudinum. Guild attributes and
Table 2
a
Epibenthic guild of amphipods
Epibenthic guild characteristic Thalassia testudinum SAV
Mean abundance (ind) 60 150
Habitat complexity 205 931 133 108
22
(mg AFDW veg m )
Density / habitat complexity 674 2355
21 205
Mean abundance, density and biomass (expressed as ash-free dry weight, AFDW) characteristics (ind) and their relationship with quantitative habitat complexity (veg) of T. testudinum and patches of Thalassia leaves
´
with attached macroalgae (SAV) from Terminos Lagoon.
attributes and quantitative physical complexity had a negative relationship in both habitats.
3.2. Predator consumption rate
Consumption rate by Farfantepenaeus duorarum on epifaunal amphipods was positively related with prey density (Table 3). Mean consumption rate fluctuated from 0.75 to 4.84 amphipods per h, indicating a variation in pink shrimp carbon ingestion
21
from 0.39 to 2.48 mg AFDW h . Consumption rate values fluctuated between treatments, and the major change was detected when two or four organisms were eaten in the fourth and the fifth treatments, respectively (Table 3). Such differences in prey consumption were more evident with the median, for two consumption groups: one group included the first four prey density treatments, while the other encompassed the three final prey densities (Fig. 2). Consumption rate was 2.6 times higher in the second
Table 3
Abundance of amphipods per aquarium in each treatment and consumption rate (Mo) of epifaunal amphipods by Farfantepenaeus duorarum at different prey density treatments in 1 h
Fig. 2. Median consumption rate (Mo) of amphipods by Farfantepenaeus duorarum in aquarium with no substrate at seven different epibenthic amphipods abundance treatments.
group than in the first. The second and fifth prey densities were selected as the experimental prey treatments in which predator effect would not be masked given their minimal variation in consumption rate (Table 3).
3.3. Habitat complexity
Consumption rate of amphipods (Mo) attributed to predation by F. duorarum decreased as habitat complexity increased in four of the five habitat conditions. Consumption rates fluctuated from 2.07 amphipods consumed in macroalgae (MA) to 1.20 amphipods in the high seagrass density (S1200) habitat, the latter was the habitat with the highest physical complexity (Table 4). The two-factor statistical analysis showed that the habitat had a significant effect on shrimp predation efficiency, while the prey density did not (Table 5). Pink shrimp consumption rate was similar in two habitat groups, the first was composed of soft-bottom substrates and macroalgae, and the second of small woody debris and low seagrass density (Fig. 3a); however, its predation efficiency was only significantly lower (P,0.05) between the former group and the high seagrass density habitat.
Table 4
Consumption rate of amphipod (Mo) caused by Farfantepenaeus duorarum in habitats with increasing physical complexity: SBS (soft-bottom substrates), SWD (mangrove small woody debris), S300 (T. testudinum seagrass
22 22
at 300 shoot m ), MA (macroalgae) and S1200 (T. testudinum at 1200 shoot m ) Habitat physical Prey mortality
complexity
Abundance (ind) (mean61 S.D.) Biomass (mg AFDW) (mean61 S.D.)
SBS 2.0561.32 1.0560.68
SWD 1.6861.14 0.8660.58
S300 1.3861.33 0.8660.68
MA 2.0761.47 1.0660.76
Table 5
Analysis of deviance results of epifaunal amphipods consumption rate (Mo) by Farfantepenaeus duorarum
a
predation in five habitats with different physical complexity and at two prey densities Source of variation Deviance df Mean deviance Fo P
Habitat 18.12 4 4.530 3.209 0.01,P,0.025
Density 4.22 1 4.220 2.989 ns
Habitat*Density 1.836 4 0.459 0.325 ns
Residual deviance 127.05 90 1.412 Total deviance 151.22 99
a
Model with interactions Mo5m 1Habitati1Densityj1Habitat*Densityij1eijk.
Interestingly, predator efficiency in macroalgae was similar to that obtained for soft-bottom substrates (Table 4), which is the habitat with the least physical complexity. This was an unexpected result assuming that macroalgae had a greater complexity structure than soft-bottom substrates. It is evident that shrimp efficiency as a predator was similar in the woody debris and low seagrasses density.
Although prey density effect was not statistically significant (F53.95, P50.0825), a skewness effect was due to a greater consumption when more preys were available (Fig. 3b). Shrimp predation intensity on amphipods was of 9% at the lower prey density and increased slightly to a 11% at the higher density. The interaction between habitat complexity and prey density was not significant (Table 5), so their effect on consump-tion rate were independent (Fig. 3c).
4. Discussion and conclusion
Amphipod species richness in three natural habitats at the study site amounted to 15 species. The absence of amphipod in soft-bottom substrates constitutes an unexpected
22
event since densities over 800 ind m have been reported in similar tropical habitats (Lewis and Stoner, 1983). In SAV there were three infaunal species identified, indicating that they use it as an alternative habitat. This suggests that infaunal amphipods can extend their range of microhabitats by using macroalgae and seagrasses blades as additional substrates. However, this does not necessarily imply that they represent food items for epibenthic predators such as F. duorarum. The species richness of epibenthic amphipods was high in both habitats composed of T. testudinum (nine and 14 species in the monospecific and SAV patches, respectively). These species were abundant and are known to be trophically important in estuarine systems (Zimmerman et al., 1979; Stoner, 1983). Amphipods may also be trophically important at ‘El Cayo’, where their density is similar to those previously reported in other estuarine coastal systems (Nelson, 1979a; Stoner, 1980).
Fig. 3. Graphic representation of amphipod consumption rate (Mo) confidence intervals by Farfantepenaeus duorarum. Confidence intervals [exphln(Mo)61.96*œVar(ln(Mo))j] are given as a function of: (a) habitat
22
[SBS5soft-bottom substrates, SWD5mangrove small woody debris, S3005seagrass at 300 shoot m ,
22 22 22
from predators, reproduction and dispersal (Jernakoff et al., 1996). Although amphipods are usually considered as mesograsers of surface perifiton on seagrass leaves and on macroalgae fronds (Nicotri, 1980; Fry, 1984; Kitting, 1984; Buschmann, 1990), our biomass values showed that T. testudinum greater carbon content does not support a higher amphipod abundance than SAV. These findings differ from the accepted concept that quantitative habitat complexity is directly related to faunal abundance and that the carrying capacity of a given substrate can be assessed by its qualitative and quantitative properties (Stoner and Lewis, 1985; Edgar, 1983). The higher rate values of either amphipod biomass or density divided by the quantitative habitat complexity revealed the higher refuge value of SAV. We contend that the above results are due to the existing relationship between the species number and the differential habitat use as a feeding or a refuge site, since these factors affect species coexistence (Zimmerman et al., 1979; Price and Hylleberg, 1982; Kitting et al., 1984). However, further studies would be required to test whether the amphipod higher abundance in SAV may be promoted by food quality and selectivity on macroalgae rather than by just food or refuge quantity.
Predation pressure in natural communities is one of the main factors that affect amphipod community structure and depends on predator foraging efficiency. The effect of this factor on any prey population structure is related to their availability and accessibility, hence the predation pressure by the pink shrimp should be focused on prey items like the epibenthic amphipod guild. In our experimental study, the F. duorarum consumption rate on amphipods indicated its ability to consume higher amphipod
22
densities than 3852 ind m without reaching a satiation point. This consumption rate increased as amphipod density did, while null habitat structure does not preclude its accessibility to the prey. Prey mortality by predation varied from 35 to 55% which falls within the value previously estimated by Nelson (1979a) for penaeid shrimp predation efficiency on macrofauna. It also reveals the regulating capacity that F. duorarum may exert upon epibenthic amphipod guilds. Estuarine epibenthic amphipods can thus represent an important food item for this predator since their nutritional value can account for predator selectivity and predation efficiency.
Predation pressure in structured habitats is additionally affected by habitat physical complexity. This applies to the pink shrimp F. duorarum, whose maximum densities occur on seagrasses beds from which they derive greater refuge and food (Gore et al.,
´
1981; Nelson and Capone, 1990; Sheridan, 1992; Sanchez, 1997).
The experimental approach to habitat physical complexity effect on predation efficiency in this study proved that both factors maintain an inverse and a non-linear relationship. Higher predation in non-structured habitats, as that recorded in soft-bottom substrates, is linked to a lack of refuge in these habitats allowing predators easy access to prey. In structured habitats, such as the seagrass canopy, refuge within the habitat allows prey to avoid predators, thus causing lower consumption rates. In seagrass beds the lower predation efficiency of fish and decapods can also contribute to cause such effect (Van Dolah, 1978; Bierbaum, 1979; Nelson, 1979b; Stoner, 1983).
design, the estimated consumption rate in woody debris and low seagrass density indicated that both habitats have a similar refuge value for amphipods. This equality was again unexpected given the more complex architecture and surface area of low seagrass density. Therefore, woody debris may be an alternative refuge similar to seagrasses at low shoot density, but its habitat value as a feeding site for amphipods and shrimp in estuarine systems is probably low (Price and Hylleberg, 1982; Kitting et al., 1984).
In seagrass meadows a positive relationship between seagrasses natural physical complexity variability and macrofauna survival has been established (Stoner, 1980; Nelson, 1981; Wilson et al., 1990; Kenyon et al., 1997). This fact was detected in our experimental treatments as a negative relationship between F. duorarum predation efficiency and the seagrass physical complexity. Predation efficiency recorded in the seagrass habitats are similar to those obtained in previous studies (Nelson, 1979b, 1981; Heck and Thoman, 1981; Main, 1987; Stoner, 1980; Stoner and Lewis, 1985), and may support the argument that higher prey survival is a function of a greater seagrass complexity, and that increments in leaf density reduces macrofauna predation efficiency. The amphipod mortality rate in macroalgae was similar to that of soft-bottom substrates. We have assumed that macroalgae represented a habitat with higher complexity than woody debris and low seagrass density. However, the high architectural complexity of macroalgae has been associated with its differential selection by macrofauna as a consequence of its higher refuge and / or feeding value (Lewis and Hollingworth, 1982; Edgar, 1983; Holmlund et al., 1990; Wilson et al., 1990). On the other hand, artificial macroalgae did not provide more refuge that the non-structured habitat and the differential use of macroalgae by amphipods described in the field by Edgar (1983), coincides with the higher amphipod distribution in SAV, than on the
´
monospecific meadows of T. testudinum in Terminos Lagoon. Amphipod distribution in SAV may promote lower predation intensity by F. duorarum due to the shrimp’s
´
recruitment preference on seagrasses (Sanchez, 1997). Our field data contrast with the high experimental amphipod mortality herein reported. It has been suggested that amphipods migrate nocturnally towards habitats like macroalgae in search for food (Edgar, 1983; Holmlund et al., 1990). Such a migration could be accountable for the higher species richness in SAV. The absence of shrimp smaller than 3 mm CL in
Lawrencia spp. during this study suggests that the macroalgae high leaf package allows
Inher-ent biological and ethological factors of the organisms involved must also be considered, coupled to spatial and temporal variations in the habitats. Thus, the relative value of any estuarine habitat can be different and may depend on behaviour, mobility and identity of prey and predator populations.
Acknowledgements
This research was funded by UNAM through the ICMyL and the DGAPA (project ´
IN211795). Specially thanks are due to our colleagues A. Raz-Guzman for her comments on the first draft of the manuscript, and S. Manickchand-Heileman for the
´
review of the English version. To Dr Silvia Ruiz-Vazquez Acosta, Institute of Research in Mathemathics Applied to Systems, UNAM for her valuable assistance in the statistical analysis. The comments and suggestions of two anonymous reviewers greatly improved this manuscript. The authors would like to thank A. Reda for his assistance in the field,
´
and to N.A. Lopez for the macroalgae identification. [RW]
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