Habitat Complexity Alters Predator-Prey Interactions in a Shallow Water Ecosystem

Abstract

Habitat complexity can profoundly influence interactions between predators and their prey due to changes to foraging efficiencies. In aquatic systems, habitat alterations can alter pursuit times and swimming behaviours of predator–prey participants, which in turn could mediate the strength of their interactions and, thus, population dynamics. The lower reaches of estuarine ecosystems are typically characterised by extensive beds of submerged macrophytes that might influence the trophic dynamics between pelagic predators and their prey. Here, we investigate the influence of increasing habitat complexity on the consumption of the calanoid copepod, Paracartia longipatella, by adult male and female mysid, Mesopodopsis wooldridgei, by means of a comparative functional response approach. Using structures that resembled aquatic vegetation, we quantified and compared feeding rates, attack rates, and handling times across the habitat gradient, and we questioned whether responses to habitat complexity are different between sexes. Feeding rates related significantly negatively to increasing habitat complexity for both males and females, with Type II functional responses consistently displayed. Functional response differed significantly across habitat complexities, with feeding rates at low and intermediate prey densities significantly greater in the absence of habitat compared to more complex structures for both predator sexes. Results of the current study demonstrate that increased habitat complexity mediates outcomes of interactions between M. wooldridgei and the calanoid copepod, P. longipatella across predator sexes, and possibly for other predators and prey in shallow waters. Owing to spatiotemporal differences in habitat structure within shallow waters, the strength of interactions in this predator–prey system likely differs in areas where they co-exist.

1. Introduction

Submerged macrophytes play a key role in the ecosystem functioning of shallow waters because they provide habitat, stabilise sediment, and act as a pelagic nutrient filter [1,2]. In addition, submerged macrophytes provide structural complexity, represent areas of increased food availability, and might afford a refuge against predation [3,4]. The decline in predation rates in the submerged beds reflects the increase in search and pursuit time and the impeding of swimming behaviour of predators [4]. Submerged macrophyte beds, therefore, play an important role in mediating predator–prey interactions, particularly within shallow water ecosystems.

The mysid Mesopodopsis wooldrigei Whitman 1992 is distributed along the south-eastern seaboard of southern Africa and forms an important component of the zooplankton community in the nearshore and lower reach estuaries within the region, where it can attain maximum densities of up to 2500 ind·m⁻³ [5,6]. Recently, it has been demonstrated [7] that M. wooldridgei preferentially consumed the calanoid copepod, Paracartia longipatella [8] over an alternative prey, irrespective of its proportional availability in the environment. Consequently, it was proposed that the mysid plays an important role in determining the distribution of P. longipatella in the lower reach of estuaries where they co-occur. However, whether the strength of this predator–prey interaction is further mediated by specific environmental contexts remains unexplored.

The strength of interactions between predators and prey have been classically quantified using a functional response approach [9]. Functional responses quantify the resource use of a consumer (e.g., predator) in relation to the density of a resource (e.g., prey), with both the magnitude and the form (typically Types I, II, and III), theoretically, proposed to mediate outcomes in relation to the stability of predator–prey groupings [10]. Functional responses have been used across numerous study systems and habitat types to quantify the influence of key environmental context dependencies on consumer–resource interactions, with generalities derived across studies. For example, temperature has been shown to illicit a hump-shaped response for the attack rate (i.e., search coefficient) and maximum feeding rate (i.e., inverse of handling time) parameters [11]. Similarly, consumer–resource size ratios have been shown to drive hump-shaped functional response parameters, with feeding efficiencies peaking at intermediate size classes [12,13].

Moreover, prey traits have been found to be more important than temperature or body size scaling for consumer–resource interaction strengths, with characteristics such as prey softness and taxonomic grouping being pervasive in driving variations in functional responses [14]. Experimental design can also influence functional response parameterisation, with increased experimental duration, for example, found to cause reduced attack rates, and handling times shown to be mediated by the extent of consumer starvation prior to feeding [15]. Furthermore, the choice of arena size can influence functional response parameters more than temperature or body size owing to effects on clearance rates [16]. In more specific systems, abiotic factors such as habitat complexity [17,18] and temperature [19] have been shown to systematically mediate interaction strengths between predator–prey participants. Furthermore, sex and reproductive status have been shown to mediate the strength of trophic interactions [20]. Nevertheless, despite these ranging context dependencies that make predictions of empirical consumer–resource dynamics challenging, quantification of functional response parameters, even in simplified laboratory settings, has been shown to be predictive of in-field interaction strengths and ecological impacts, whereby greater attack rates, shorter handling times, and higher maximum feeding rates are conducive to greater consumptive effects [10,20,21]. Thus, the comparative use of functional responses can provide useful phenomenological insights into the effects of pertinent current and future environmental contexts on trophic dynamics. However, for many species and study systems, the strengths of trophic interactions lack examination, hampering predictive efforts surrounding the effects of habitat degradation and climate change.

In an estuarine context, the presence of submerged macrophyte beds in the lower reaches suggests that these plants play an important role in mediating the interactions between pelagic predators and their prey. The trophic dynamics in these systems generally lack investigation, and effects of habitat structure might manifest differently according to key demographics such as sex. Therefore, to assess the influence of increased habitat complexity on the consumption of two key species, the calanoid copepod, P. longipatella, by adult male and female mysid, M. wooldridgei, we used a functional response approach. We hypothesised that increased habitat complexity would reduce functional responses between predator and prey, with subsequent alterations to feeding rates. We also anticipated feeding responses to be similar between predator sexes as we did not consider reproductive status.

2. Materials and Methods

2.1. Experimental Setup

Zooplankton were collected from the lower reach of the permanently open Kariega Estuary in the Eastern Cape Province of South Africa (33°68′06.0″ S; 26°26′67.0″ E) on 27 February 2005 by trawling a WP-2 net (diameter 50 cm; 100 μm mesh) through the water column 1 h after sunset. The zooplankton collected were transported in source water to a controlled environment (CE) room and maintained under ambient conditions (18.5 ± 0.5 °C under a 14:10 light: dark regime) at Rhodes University, South Africa. In the CE room, adult M. wooldrigei were isolated from the smaller zooplankton, comprising mainly copepods, and stored in aerated 25 L aquaria containing 50 μm-filtered water from the source. Feeding experiments were conducted in 2 L arenas filled with source water, which had been gravimetrically filtered through a 50 μm sieve to remove all metazoans. To simulate natural vegetation, we used green plastic strips of 3–5 mm width and 12–15 cm length attached to a plastic mesh secured to the base of the arena. The structure of the artificial vegetation employed during the study mimics that of Zostera capensis, which has extended its distribution along the entire length of the estuary due to reduced freshwater inflow into the system. Densities of plastic strips ranged between 8 and 12 strips per cm² that extended to within 2 cm of the surface. Artificial vegetation was prepared 2 days prior to the feeding studies and was stored in source water. Adult mysids were fed ad libitum on adult P. longipatella for 3 days prior to the start of the feeding experiments. Adult mysids were starved for 24 h prior to the start of the feeding study.

To assess the influence of habitat complexity on interaction strengths from the mysid, we quantified the predation rate of M. woolridgei towards five different densities of the copepod P. longipatella (5, 10, 15, and 20) at five different levels of complexity (0%, 25%, 50%, 75%, and 100% cover). Densities correspond to individuals per arena (2 L volume). We acknowledge that lower predator densities than applied here could have allowed better resolution in distinguishing functional responses where prey are rare, and higher densities could have permitted a clearer asymptote under certain treatments (see later), but the selected range is nevertheless comparable among treatment groups. Vegetation coverage was determined as the percentage of the area of artificial plants relative to the bottom area of each arena. Individual adult prey (total length (TL) 0.65–0.82 mm) were introduced into the arenas using a dropper. After prey had acclimated for 4 h in the experimental arenas, a single male (TL 11–14 mm) or female M. wooldridgei (TL 9–13 mm) was gently introduced into each arena, and then allowed to feed for 24 h. Three separate arenas (i.e., replicates) were prepared for each predator sex and habitat type, and controls consisted of three replicates fitted with a grid in the absence of predators for each level of artificial vegetation. After the experimental period, each mysid was removed using a small handheld net, and the water in the arena was gently filtered through a 20 µm mesh to isolate the remaining live prey. Changes in prey number were assumed to reflect prey mortality from predation.

2.2. Statistics

Binomial generalised linear models with logit links were used to examine proportional prey consumption (i.e., eaten vs. alive) at the end of the feeding experiment. Predator sex (two levels), habitat complexity (five levels), and prey density (continuous) were included as predictor variables, with all interaction terms included in an initial, full model. We followed a step deletion procedure based on analyses of deviance, whereby terms were removed in order of significance, with higher-order interactions (i.e., three- and two-way interactions) successively removed first [22]. Accordingly, the final model included only significant terms at the 95% level. Type II analysis of deviance was used to infer effect sizes in the final model [23], using likelihood ratio chi-square tests. Post hoc pairwise Tukey tests were used, where appropriate, using least square means [24]. All statistical analyses were performed in R v3.5.1 (R Development Core Team, 2018).

Functional response types for each predator and habitat treatment group were tested separately (n = 10) using logistic regression (i.e., binomial generalised linear models) considering proportional prey consumption (as above) as a function of prey density (continuous). A significant negative first-order term indicates a Type II (the proportion of prey consumed declines monotonically with prey density) functional response, whilst a significant positive first-order term, followed by a significant negative second-order term, indicates a Type III (the proportion of the prey consumed is positively density-dependent at initial prey density, before again declining in rate) functional response [25]. Where functional response types were equivocal (i.e., nonsignificant terms), multiple models were fit to the data (Types II [26], III [27], and flexible (i.e., with scaling exponent; [28]), and model selection was based on Akaike information criterion (AIC) comparisons. AIC is a mathematical method for evaluating how well a model fits the data it was generated from, where lower values indicate a better fit) [29]. Flexible functional response models allow for a continuum between Types II and III through the inclusion of a scaling exponent, q (values closer to 1 indicate an increasingly Type III form). We considered models with ΔAIC < 2 to be interchangeable [30]. Owing to non-replacement of prey consumed, we fit the random predator equation proposed by Rogers to each dataset separately [26],

$$N_e=N_0(1-\exp \left(a\left(N_{e}h-T)\right)\right)m$$

(1)

where N_e is the number of prey eaten, N₀ is the initial prey density, a is the predator attack rate (classically interpreted as the search efficiency), h is the predator handling time (defined as the time spent pursuing, subduing, and consuming each prey item plus the time spent preparing to search for the next prey item), and T is the duration of the experiment. The Lambert W function was employed to allow for model fitting, since N_e appears on both sides of the equation [31]. To compare functional responses across prey densities, initial parameters (attack rate, a; handling time, h) were nonparametrically bootstrapped 2000 times to propagate 95% confidence intervals around curves. Using the original parameters from Equation (1), this approach computes the likely range of fitted coefficients and allows for direct comparison of the fitted values [29]. Bias-corrected and accelerated intervals were used to account for potential skew and bias in the estimates. Differences in functional responses across prey densities were, therefore, based on a comparison of the presence or absence of confidence interval overlaps across prey densities, because the bootstraps can be considered as population-level as opposed to sample-level metrics [29]. Whilst comparisons of functional responses based on bootstrapped confidence intervals alone have been proposed to be a sufficient means of statistical difference inference [17], we additionally analysed bootstrapped parameters (a, h) separately using Gamma generalised linear models with log links, as a function of predator sex (two levels), habitat complexity (five levels), and their interaction. Type III sums of squares were used to quantify effect sizes, owing to the presence of interaction terms in the final model [23].

3. Results

A mean of 84% (±SD = 10.5%) of prey survived across predator-free control treatment groups. Control survival rates did not differ significantly across predator or habitat treatment groups (binomial generalised linear model: predator, χ = 1.40, df = 1, p = 0.24; habitat, χ = 4.07, df = 1, p = 0.40; predator × habitat, χ = 0.96, df = 4, p = 0.92). Considering proportional prey consumption, the final, most parsimonious model included habitat complexity (χ = 36.05, df = 4, p < 0.001) and prey density (χ = 55.62, df = 1, p < 0.001) as singular terms, with proportional consumption relating significantly negatively to increasing prey density overall (Figure 1). A significantly greater proportion of available prey was consumed under the 0% complexity treatment as compared to complexities of 50% or higher (all p < 0.05). In turn, significantly greater consumption rates were exhibited under 25% complexity as compared to 75% and 100% (both p < 0.05). Predator sex was not a significant determinant of raw consumption rates (χ = 0.01, df = 1, p = 0.91), across all habitat complexities and prey densities, because all interaction terms were nonsignificant and, thus, removed stepwise (all p > 0.05). In other words, prey consumption rates by mysid predators declined as prey densities increased, and these effects were similar between males and females.

First-order terms (i.e., linear coefficients) were significantly negative across the majority of predator and habitat complexity treatments (

Table 1. Mesopodopsis wooldridgei functional response first-order terms, attack rates, and handling times across predator sex and habitat complexity treatments, along with associated p-values. Significant p-values are emboldened.

Sex	Habitat	First-Order Term, p	Attack Rate, p	Handling Time, p
Female	0%	−0.14, <0.001	6.33, 0.15	0.16, <0.001
	25%	−0.07, 0.05	1.33, 0.06	0.11, 0.01
	50%	−0.07, 0.04	1.01, 0.07	0.12, 0.02
	75%	−0.04, 0.26	0.46, 0.06	0.11, 0.27
	100%	−0.04, 0.28	0.65, 0.15	0.13, 0.18
Male	0%	−0.12, <0.001	3.65, 0.09	0.14, <0.001
	25%	−0.09, 0.01	1.99, 0.14	0.15, <0.001
	50%	−0.11, 0.002	2.29, 0.20	0.18, <0.001
	75%	−0.06, 0.14	0.62, 0.12	0.15, 0.11
	100%	−0.07, 0.05	0.86, 0.12	0.16, 0.03

), except for three treatments (female: 75%, 100%; male: 75%). This meant that most functional responses were deemed Type II, irrespective of habitat type and predator sex, with feeding rates declining with increasing prey density. However, in equivocal cases (see before), comparison of AIC yielded evidence for minimal information loss via Type II models in comparison to Type III and flexible alternative models that included a scaling exponent. Thus, the Type II model (Equation (1)) was ultimately used for all treatments, aligning with high consumption rates at low prey densities by predators in all instances.

For both males and females, prey attack rates tended to fall concurrently with increasing habitat complexity (Table 1), whilst prey handling time effects were less consistently affected by habitat levels (Table 1). Bootstrapped attack rates and handling times differed significantly across habitat levels, an effect that significantly interacted with predator sex (a, χ² = 211.51, df = 4, p < 0.001; h, χ² = 1045.52, df = 4, p < 0.001). Confidence intervals were divergent and, thus, differences were statistically clear for female predators at 0% complexity compared to higher habitat levels (50%, 75%) at low–intermediate prey densities (i.e., functional response slope), and at 100% complexity at intermediate densities, yet they always overlapped across all treatments at high densities, indicating a lack of statistically clear differences (Figure 2a–d). For males, confidence intervals at 0% complexity were divergent and significantly different in relation to those at 75% under low–intermediate prey densities, and at 100% complexity at intermediate densities (Figure 2e–h). Confidence intervals for males always overlapped at the highest prey densities, indicating a lack of significant differences. Therefore, habitat complexity effects on predation were prey density-dependent, yet generally similar between predator sexes.

4. Discussion

The present study quantified the effect of habitat complexity on the consumption of two key estuarine species, the calanoid copepod, P. longipatella, by adult male and female mysid, M. wooldridgei, in a laboratory experiment using a functional response approach. Feeding rates were significantly affected by both habitat complexity and prey density; however, they were relatively consistent according to predator sex. Habitat complexity generally reduced the efficiencies of predators; these effects were, in turn, dependent on prey density. Type II functional responses were similar for male and female mysids owing to their consistently high prey acquisition at low prey densities; thus, both these sexes could extirpate prey populations at low densities irrespective of habitat. Attack rates of both sexes of the mysid generally decreased in response to increased habitat complexity, with habitat effects, thus, most pronounced at low prey densities. In contrast, handling times of both sexes of the mysid undulated in response by habitat complexity, whilst maximum feeding rates were similarly variable. It is worth noting that both habitat complexity and predator density play an important role in predator–prey dynamics [32]. While our study only included a single predator, the main findings of the study provide important insights into the role of habitat complexity in mediating the interaction between the mysid and the copepod, and predator–predator interactions among conspecific mysids have been shown to combine additively [33].

The effect of habitat complexity in altering the feeding rates of predators has been studied in a limited number of shallow water aquatic systems [20,34]. Results of these investigations indicate that the emergent effects of habitat complexity are largely a function of predator feeding mode [32]. For those predators that actively pursue their prey, increases in habitat complexity are normally associated with decreased feeding rates as a result of the increased pursuit and search time and the impeding of swimming [32,35]. By contrast, for sit-and-wait/ambush predators, increased habitat complexity is usually accompanied by increased feeding efficiency [36,37]. These effects on search efficiency are likely to manifest as differences in attack rates, which correspond to the initial slope on functional response curves. These effects are, however, also contingent on a number of factors, including relative predator–prey body size scaling and behavioural responses of prey, which can alter functional response parameters [38]. Mysids are active, raptorial predators that employ visual cues to locate their prey [39]. The significant decrease in attack rates of both sexes of the mysid in response to increased habitat complexity is, thus, expected. The mechanisms underpinning the decrease in functional response attack rates are unknown; however, considering the active swimming behaviour of the mysid, it is likely that the increased cover of artificial macrophytes would have impeded their swimming and additionally afforded the copepod some refuge from predation via reduced encounter rates. Similarly, whilst prey handling times (including time spent digesting prey) undulated across different complexity levels in the present study, the explanation for this specific pattern is unknown.

Both male and female M. wooldridgei exhibited a Type II functional response towards the calanoid copepod, P. longipatella, across the habitat complexity gradient. The predatory effect of the mysid towards the copepod might, therefore, be largely unaffected by habitat complexity where they co-exist, with Type II functional responses typically thought to be prey-destabilising [10]. That is, consumers which exhibit high rates of prey consumption at low densities, conducive to Type II functional responses, are thought to limit any potential for low-density refuge effects that could otherwise promote the stability of prey populations. In other systems, the presence of habitat complexity has been found to cause a sigmoid Type III functional response, whereby consumption rates are reduced at low prey density; hence, prey benefit from a low-density refuge due to the provision of predator-free spaces [40]. Thus, in the present study, M. wooldridgei exhibited per capita predatory effects across a habitat gradient that might destabilise prey populations because functional responses were always Type II. Nevertheless, choice of experimental prey densities and other factors might also influence functional response types, with low-density resolution important for differentiating curve types.

Furthermore, given that, during swarming events, M. wooldridgei can attain densities of up to 2500 ind·m⁻³ [5,6], it is possible that they may extirpate P. longipatella in the lower reach of estuaries where they co-occur, given the importance of consumer abundance and functional response for ecological impacts [10]. This observed pattern is consistent with a number of previous studies conducted in temperate ephemeral ponds within the same geographic region [19,21]. The result is, however, in contrast to a recent meta-analysis which indicated that crustaceans generally exhibit a Type III functional response with an increase in habitat complexity [41]. Since the Type III response is stabilising due to low predation pressure at low prey densities [42], crustaceans were, therefore, suggested to be unlikely to contribute to localised prey extinction. Since handling times of both sexes of mysid were not consistently affected by habitat complexity, maximum feeding rate effects were also inconsistent. Again, this result is in contrast to a recent study which demonstrated that the sex demographics of crustaceans alter the effect of habitat structure on predation rates [21]. That said, the present study did not consider reproductive state, which has previously been shown to play an important role in mediating predator–prey outcomes [20].

Results of the study demonstrated the interplay between habitat complexity and predation success of the mysid M. wooldrdgei on the calanoid copepod P. longipatella. Wasserman et al. (2016) demonstrated that there was a multifaceted interaction between habitat complexity and temperature, which contributed to changes in the handling times of predators in ephemeral pond systems in southern Africa. Shifting temperatures are also implicated in destabilising predator–prey interactions by shifting functional responses [43]. Given that water temperatures in the lower reach of estuaries demonstrate strong temporal variation due to tidal regimes, future investigations should consider the interplay between habitat complexity and temperature in mediating the interactions between the predatory mysid, M. wooldridgei, and its preferred prey, the calanoid copepod, P. longipatella. These variabilities are exacerbated since global warming will contribute to increases in global seawater temperatures. It is probable that warming will intensify predator–prey interactions up to a given thermal optimum [44], and the accompanying effects on dissolved oxygen will further mediate interactions [45]. The influence of temperature and dissolved oxygen in mediating the strength of predator–prey interactions between the mysid and copepod was, however, beyond the scope of the current investigation. Nonetheless, our study, using predator and prey densities recorded under natural conditions [6], provides invaluable insights into the role of structural complexity conferred by submerged macrophytes in mediating the interaction between the mysid and its preferred prey.

Submerged macrophytes provide a habitat for a variety of invertebrates and vertebrates, stabilise sediments, and act as a pelagic nutrient filter [1,2]. Results of the current investigation indicate that the habitat complexity also plays a pivotal role in mediating the strength of the predator–prey interaction between the mysid, M. woolrdgei, and the copepod, P. longipatella. These findings highlight the need for the conservation of submerged macrophyte beds in estuaries since they play an important role in the ecosystem functioning of these systems.