Effects of predators on reef fishes: separating cage artifacts from effects of predation

JOURNAL OF EXPERIMENTAL MARINE BICLGGY AND ECOLOGY

Journal of Experimental Marine Biology and Ecology,

ELSEVIER

198 (1996)

249-267

Effects of predators on reef fishes: separating cage artifacts from effects of predation Mark A. Steele* Departmentqf Biological

Sciences,

University

of Californiu.

Sanra

Burbara,

CA

93106,

USA

Received 28 August 1995; revised 1I December 1995; accepted 12 January 1996

Abstract Predators are thought to play prominent roles in determining population abundance and dynamics of many species, but it is often difficult to document effects of predators in the held. For lack of any other effective means of manipulating predator densities, many studies use predator exclosures, however, the results of these studies are difficult to interpret because the exclosures may introduce artifacts that cannot be separated from predatory effects. Using a design common in tests of predatory effects, exclosure cages ( - predators), “cage controls” = partial cages ( + predators), and no cages ( + predators), patterns of survival were found for two reef fishes that were consistent with both predator and cage effects. To separate cage artifacts from effects of predators, direct tests of cage effects in an environment free of predators were conducted, within a large predator exclosure. Cage artifacts had dramatic effects on one fish species but not the other. Moreover, the way the affected species responded to cages was exactly what would be expected if predators had strong negative effects on these fish: growth and survivorship were much lower on uncaged reefs than on caged reefs. To circumvent the cage effects, rather than compare uncaged reefs ( + predators) to reefs in exclosure cages (predators), exclosures were compared to partial cages ( + predators). In the absence of predators, the partial cages did not differ from exclosure cages in their effects on the prey. Using the partial cages and exclosure cages in an area where predators were present, predator effects on the two fishes were tested. Survivorship of one species was greatly reduced by predators, but the other species was not affected. The lack of a predator effect on the one species was apparently an artifact of comparing completely caged reefs to partially caged reefs; another experiment documented strong predator effects on this species. Partial cages probably greatly reduced the ability of predators to consume the “unaffected” species. When cage artifacts affect prey, partial cages may be usefully employed to avoid confounding predator effects with cage effects at the cost of underestimating the magnitude ol predator effects. Direct tests of cage effects are necessary to interpret the results of any study that uses cages to test for predatory effects. Keywords: hsh

Cage effects;

Cmyphopterus

nicholsii; Exclosures;

Lythrypnus

*Corresponding author. Fax: (1) (310) 206-3987. 0022-0981

P/I

/Y6/$15.00

SOO22-OY81(96)0001

0

1996

Elsevier Science B.V. All rights reserved 1-I

dulli; Predation;

Reef

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1. Introduction Predation is believed to be one of the main processes structuring populations and communities. Predators have been found to affect numerous diverse organisms, in a population densities and variety of ways (e.g., effects on behavior of individuals, population dynamics; for review, see Sih et al., 1985). In many systems, however, unambiguously demonstrating predator effects has proven difficult. This difficulty usually stems from logistical problems associated with manipulating predators, or from problems interpreting the results of studies that successfully manipulated predator densities. These problems have especially plagued studies of reef fishes (for review, see Hixon, 1991), and hence, the extent to which reef fish populations are affected by predators remains uncertain. In this study the effects of predators on two temperate zone reef fishes are explored. One of the most straightforward ways to demonstrate that predators affect the density or dynamics of a prey population is to manipulate the density of predators and then document a response by the prey population. Ideally, this may be accomplished by simply removing predators. However, in many systems this technique is ineffective because the high mobility of the predators results in no effective decrease in predator density (e.g., Stimson et al., 1982; Caley, 1993). In such systems a more practical approach is to surround prey populations with barriers, usually cages, that are impermeable to predators, thereby ensuring that manipulations of predator density will be maintained. Cages can be used to manipulate predator density in two different ways: (1) predators (P) may be excluded ( - P) from certain areas by cage exclosures, and prey populations in these areas are then compared to populations in areas where predators are not excluded ( + P), or (2) predators may be enclosed in caged areas ( + P; potentially over a range of densities) with prey, which are then compared to caged areas that exclude predators ( - P), but include prey. The main problem with the first approach is that any effects predators have on prey may be confounded with effects of the cages themselves. The second approach does not suffer this problem because all prey populations are enclosed in cages, so any differences between predator treatments may be reliably attributed to predators and not cages. However, because predator behavior may be altered by confinement in a cage, it is not always clear how results of cage enclosure experiments relate to the effects of predators under natural conditions. This is more of a problem when the predators of interest are highly mobile and/or large in size relative to the enclosure, in which case, enclosure experiments are not recommended (Dayton and Oliver, 1980; Choat, 1982). For relatively sedentary predators, enclosure studies may be more useful (e.g., Walde and Davies, 1984). Ecologists interested in exploring the effects of highly mobile predators, such as many of the predatory fishes that consume reef fishes, may have no recourse but to conduct studies using exclosures. While this approach suffers from a variety of shortcomings (e.g., inability to expose prey populations to a wide range of predator densities to generate prey response curves), perhaps the biggest problem is that the exclusion device may affect the prey in unintended ways, thus confounding “cage effects” with those of predators (Virnstein, 1977, Virnstein, 1978; Peterson, 1979; Dayton and Oliver, 1980;

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Hurlberg and Oliver, 1980; Schmidt and Warner, 1984; Underwood and Denley, 1984; Walde and Davies, 1984; Peckarsky and Penton, 1990). Frequently cage effects are addressed by incorporating some sort of “cage control” treatment which is meant to simulate all the effects of the exclusion device without excluding predators. This “control” is often a partial cage that allows mobile predators some access to the interior. The “cage control” treatment is then compared to completely uncaged areas with the hopes that no difference will be found between the two treatments, presumably demonstrating that cages had no effects on the prey. This approach has two weaknesses: ( 1) it is impossible to create a cage control that is exactly the same as the cage, so even if the cage control has no effects, this finding does not demonstrate that cages have no effects and (2) often, “cage controls” have effects intermediate between caged and uncaged treatments (e.g., Schmidt and Warner, 1984). This may indicate that cages, and not predators, affect prey, because “cage controls” would not be expected to affect prey as strongly as full cages, since they are actually intermediate in design between cages and uncaged areas. Alternately, intermediate effects of cage controls could indicate that predators actually do affect prey, and that cage controls simply reduce accessibility of prey to predators, relative to uncaged areas. Intermediate effects are probably commonly caused by a combination of cage effects and intermediate exposure of prey to predators. In cases where no other information is available, it is impossible to disentangle the two alternate explanations, and hence, the actual effects of predators remain unknown. A more straightforward way to evaluate potential cage artifacts is to directly test for them. This obvious approach is rarely used (but see Kennelly, 1983, Kennelly, 1991). presumably due to the potentially large investment of time and energy required to carry it out. However, as will be argued below, the information gained from such tests may be crucial. Here, a set of experiments conducted to test the effects of predators on two temperate zone reef fishes, and to explore artifacts associated with different cage designs is described. An experiment to test for predator effects using the standard cage ( - P), “cage control” ( + P) and no cage ( + P) design was conducted first. Because of the previously mentioned interpretation problems associated with this design, a direct test of cage artifacts was carried out on the two prey species, in the absence of predators. The results of that study spurred me to design a structure that allowed predators access to prey, but that affected the prey no differently than the exclosures did. In the absence of predators, differences between the new predator-accessible structures and exclosure cages were tested with respect to their effects on prey. The two structures were then used to test for predatory effects on populations of the two fishes.

2. Methods 2. I. The study system All experiments were conducted in Big Fisherman Cove, Santa Catalina Island, USA (33”27’N, 118”29’W). Two common benthic reef fishes were used, the bluebanded goby (Lythrypnus dulli Gilbert) and the blackeyed goby (Coryphopterus nicholsii Bean). Both species are small ( < 10 cm standard length (SL) for Coryphopterus and < 5 cm for

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Lythrypnus), relatively sedentary, and primarily planktivorous. Lyth~~pnus reaches densities as high as 120 m -’ while never more than 20 Coryphopterus are found in a I m* area (M.A. Steele, unpublished data). At Santa Catalina Island, the two gobies are mostly preyed upon by the serranids Paralabrux clathrutus Girard (kelp bass) and P. nebulifer Girard (barred sand bass). A few labrids (Semicossyphus pulcher Ayres, Halichoeres semicinctus Ayres, Oxyjulis californica Giinther) that usually consume invertebrates may occasionally consume the gobies. Other potential predators are probably too rare at the study site to have any significant effect on populations of the two gobies. 2.2. Experiment I: Standard and uncaged reefs

test for effects of predators:

cages,

“cage controls ”

To explore the effects of predators on the survivorship of the two species of gobies, an experiment was initiated on August 28, 1991 which lasted for 6 weeks. Groups of gobies (ten of each species, see below for details) were stocked on replicate rock rubble reefs, enclosed in (1) predator exclosure cages ( - P, Fig. la), (2) “cage controls” ( + P, cage frames covered only on the top half with netting, Fig. lb) and (3) on uncaged reefs ( + P, Fig. lc; see Fig. 1 for designs of all predator manipulation treatments and Table 1 for a summary of each experiment). Exclosure cages were 1 m’ and covered on all sides by 6 mm mesh cloth netting, except for the bottom third of one side which was covered by 19 mm mesh rigid plastic netting (Fig. la). This large mesh panel allowed the gobies to move on or off reefs at will. It was necessary to allow the gobies to leave the predator

a) Exclosure Cage

b) Cage Control

d) Exclosure Cage

e) Open Cage

Fig. I. Types of structures

used in tests of predator

c) No Cage

f) No Cage (Frame) and cage effects.

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Table I Design of experiments Experiment

Predators

Treatments

I 2A 28 3A 3B 4

Present Absent Absent Absent Absent Present

Cage Cage Cage Cage Cage Cage

Letters in parentheses

refer to diagrams

(a), (d) (d) (d) (d) (d)

Duration (days)

compared partial cage (b) v. frame (f) v. frame (f) v. partial cage v. partial cage v. partial cage

of each treatment

and no cage (c)

44 14

(e) (e) (e)

14

I I 25

in Fig. I.

exclosure reefs so that emigration from partially caged and uncaged reefs was not confounded with mortality caused by predators. Based on observations made over the course of the experiment, all predatory fish > 80 mm SL were excluded from exclosure cages. It is possible that predators 5 80 mm could have eaten some of the gobies on caged reefs, but this is unlikely because the only predators 5 80 mm that are capable of consuming gobies as large as those used in this experiment are the kelp and barred sand basses (pers. obs. and unpubl. data), and no basses this small were observed at the study site during the experiment. Divers scrubbed fouling material off the exclosure cages and “cage controls” at least once a week; during these disturbances, the gobies did not leave the experimental reefs; rather they took refuge in the rock rubble on the reefs. Nine, 1 m2, rock rubble reefs were constructed in = 6 m of water over a sand bottom. Each reef was constructed of a standard volume (40 1) of rocks (5-20 cm) to minimize differences in shelter availability. These rubble reefs mimicked rubble patches on nearby natural reefs, which are interspersed among areas of larger boulders and sections of solid rock. The reefs were constructed in a line parallel to a large continuous rocky reef 10 m distant, and each reef was separated from the next by 10 m of sand. Reefs were separated by 10 m of sand to minimize movement of gobies among reefs, which would confound mortality and migration (see below). Each of the nine reefs was constructed upon the bottom of an open fiberglass reinforced bag (1 X 1 mm mesh). Using some of the rock rubble, the walls of each bag were secured flush with the sand bottom around the perimeter of each reef. At the end of the experiment, the gobies were collected by raising the walls of each bag to enclose the reef, then, all but a few rocks were removed (to which the gobies aggregated), and the mouth of the bag was closed. Some resident gobies were probably lost using this collection technique, but this loss should not have been biased among treatments. The reefs covered a gradient in proximity to the mouth of Big Fisherman Cove, and it was suspected that the gobies might be affected by this gradient. To avoid having most of the replicates of any given treatment in a “good” or “bad” area, rather than assign treatments to reefs randomly, the treatments were assigned systematically, in the order; cage, “cage control”, uncaged reef. Each treatment was replicated three times. On one dive, all nine reefs were stocked with 10 L~hr_vpnu.s (20-34 mm SL) and 10 Coryphopterus (24-40 mm SL). Standard distributions of sizes were used for each species. After 44 days, gobies residing on the reefs were collected by divers and later measured to the nearest mm (SL). Based on size and known growth rates (M.A. Steele.

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unpubl. data) the gobies captured were categorized as recruits (individuals that settled during the experiment) or post-recruits. Very few gobies of either species recruited during the experiment (nine Coryphopterus recruits and zero Lyth~pnus recruits). Survivorship of the gobies was calculated as the number of post-recruits recovered divided by the number of fish stocked on each reef. This assumes that all post-recruits were fish that were stocked on the reefs, and that all tish missing from the reefs died. Hence, the measure of survivorship was confounded by successful migration to and from the reefs. However, successful migration was probably rare: in a separate studies done over 2%day periods, < 1% of either species moved among similar rubble reefs that were separated by 10 m of sand (Steele, 1995). Most gobies that attempt to move among reefs separated by 2 10 m of sand are probably eaten by predators while crossing sand (personal observations). One-way ANOVAs were used to compare survivorship of each of the two goby species among the three treatments. Prior to analysis, the assumption of homogeneity of variances was checked using Cochran’s test: this assumption was not violated for either species (P > 0.05). It was difficult to assess the assumption of normality because of the small sample sizes for each treatment, but examination of normal probability plots indicated that violations of this assumption were not gross, and ANOVA is robust to violations of this assumption when variances are homogeneous and sample sizes are equal, as they were in this experiment (Day and Quinn, 1989). 2.3. Experiment of predators

2: Effects of cages: caged ree$y versus ,frumed reefs in the ubsence

2.3.1. Experiment 2A: Effects of cages on density, growth and behavior The potential for cage effects on the density, growth and behavior of the two prey fishes was explored in an experiment conducted within a large predator-free exclosure. Groups of gobies were placed on replicate (n = 2) rubble reefs within cages, or on reefs surrounded by frames with no netting on them (Fig. Id and If). Fouling material was scrubbed from the cages at least once weekly. For logistical reasons, Experiment 2 was conducted at a different location in Big Fisherman Cove than was Experiment 1. Four 1 m’ rock rubble reefs were constructed on a sand bottom in 5 m of water. Replicate reefs were again constructed of = 40 1 of rock rubble, composed of 64 rocks (standard numbers in three size classes) ranging in length from 5 to 30 cm to minimize variability in habitat quality among reefs. To create a predator free environment, the rubble reefs were enclosed in an 8 m diameter net (Atlas 5 mm mesh). This mesh size excludes all known predators of the gobies. The bottom of the net was anchored to the sand bottom with rocks and concrete blocks, and the top was buoyed to the surface. The top of the net was tied shut to keep piscivorous fishes from entering the exclosure. The four replicate reefs were slightly > 1.5 m apart. The nearest edges of the reefs were 1 m from the net (Fig. 2). Two reefs were enclosed in complete predator exclosure cages and two were surrounded only by frames. The cages were 1 m X 1 m X 0.67 m high, and constructed of 22 mm diameter PVC pipe covered on all sides by 19 mm mesh rigid plastic netting. Gobies could move onto or off reefs at will. Reefs of one type were adjacent to two reefs

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Net barrier \ _____------___

8m

‘\ ‘,

‘\.. ‘-.

I

\ ,

,’

/’

,/’

--__ --_______---

__.’

completely

caged reef

predator accessible reef (frame or open cage) Fig. 2. Arrangement

of replicate

reefs within the large predator

exclusion

net

of the other type (Fig. 2). 30 Lythrypn~ls (2 l-29 mm SL) and ten Coryphopterus ( 19-28 mm SL) were released onto each replicate reef. Unequal numbers of the two species were used to more accurately represent the relative abundance of the two species on natural reefs. After 2 weeks, all of the gobies remaining on the reefs were collected by divers using handnets and the anesthetic quinaldine; the number of individuals remaining on each reef was recorded and apparent survivorship was estimated as the number of fish remaining divided by the number of fish stocked. Because of the short distances separating the reefs from one another and from the rocks and concrete along the base of the large net, it was probably easy for gobies to emigrate from the reef they were placed on, without suffering any mortality. As such, apparent survivorship in this experiment which was probably primarily should more accurately be considered persistence, affected by behavioral decisions by the gobies to remain on the reef they were placed on, or move elsewhere. While, upon release, none of the fish were observed to move from the intended reef to any other reef, the fish on each reef were tatooed with a unique color of acrylic paint so that their subsequent movement could be detected among the reefs. The tattoos also indicated the standard length (to the nearest millimeter) of each goby at the start of the experiment and, at the end of the experiment, each fish was remeasured to determine its growth over the period. Standard distributions of sizes were used for each species because body size influences growth rate in these two species (Steele. 1995). Focal individuals were observed over 10 min periods by divers resting motionless on the bottom = 1 m away from the reef. Foraging behavior (number of bites min- ‘; n = 2 focal individuals/species per reef), intraspecific aggressive behavior (number of attacks made or received min- ’ ; n = 2 focal individuals/species per reef), and use of shelter (fraction of time spent perched on top of rocks, potentially exposed to predators; n = I

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focal individual/species per reef) was recorded. So that the fraction of time that each goby spent perched on top of rocks could be calculated, divers recorded the time, to the nearest second, at the beginning and end of each behavior. Foraging and aggressive behavior were recorded as the number of acts/l0 min. period. When behavioral observations were made, fish were observed on all four reefs within a 1 h period. Differences between caged and framed treatments were tested for with t-tests. For analysis, all data that were proportions were arcsin-square root transformed.

2.3.2. Experiment 2B: Short-term density responses to cages To ascertain whether differences in density of Lythrypnus between caged and framed reefs (see Section 3) developed rapidly, an experiment was conducted that lasted only 1 day. Using the same reefs and methods as above, the fraction of stocked individuals that remained on the two reef types after 24 h was compared. Fish were not tattooed and behavior and growth of Lythrypnus were not examined. No Coryphopterus were stocked because Experiment 2A indicated that this species showed no cage effects (see Section 3).

2.4. Experiment 3: Tests for differences cages in the absence of predators

between effects of exclosure

cages and open

Experiment 2A demonstrated that cages affected Lythrypnus but not Coryphopterus (see Section 3). This indicated that if tests for predator effects were carried out by comparing responses of Lythrypnus on caged reefs to those on uncaged reefs, predator and cage effects would be confounded. To avoid confounding the two types of effects, structures were designed that would allow predators access to Lythrypnus but which, it was suspected, would not differ from exclosure cages in their effects on the prey. The predator-accessible structures designed were “open” cages: cages that lacked netting on the lower half of one side of the cage (Fig. le). Other than the open side, these cages did not differ from the exclosure cages, which were the same as those used in Experiment 2 (Fig. Id). Tests for differences in the effects of the two types of structures on Lythrypnus in the absence of predators, were carried out by using the large net exclosure previously described. Growth, behavior and apparent survivorship were examined in a 2-week experiment (Experiment 3A), and apparent survivorship was explored in a l-day experiment (Experiment 3B). No Coryphopterus were stocked on the four replicate reefs because Experiment 2A indicated that this species was not subject to cage effects (see Section 3).The same numbers of Lythrypnus were stocked on the reefs as in Experiment 2, but, because the range of sizes had increased on natural reefs, a slightly larger range of sizes was used than in the previous experiments: 16-33 mm SL. Behavioral observations were made in the same manner as described for Experiment 2, except that observation periods were only 5 min, and seven focal individuals were observed on each reef: four individuals were observed on one day and three on another. All other methods used were the same as described for Experiments 2A and 2B.

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2.5.

Experiment

4: Effects of predators

198 (1996) 249-267

on Lythrypnus

37

and Coryphopterus

The results of Experiment 2 demonstrated that Lythrypnus were strongly affected by cage artifacts (see Section 3), but the results of Experiment 3 indicated that predator effects could be tested for, without confounding them with cage effects on Lythrypnus, by comparing goby performance in the “open” cages ( + P) versus the exclosure cages ( - P) used in Experiments 2 and 3. Using these two treatments, tests for predator effects were carried out on the two species of gobies. This test for predator effects was made in the context of a large multifactorial experiment which also explored intra- and interspecific competition in the gobies (Steele, 1995); results concerning competition will be presented elsewhere. In this experiment, 36 rubble reefs were used, identical to those used in Experiments 2 and 3, constructed in a grid pattern with 10 m of sand separating adjacent reefs. Three rows of twelve reefs were constructed at different distances (10, 20 and 30 m) from a nearby large natural reef. Replicates of treatments were equally divided among the three rows of reefs. Treatments consisted of five combinations of different numbers of the two gobies (0 + 0, 0 Coryphopterus + 30 Lythrypnus, 0 Coryphopterus + 60 Lythrypnus, 15 Cotyphopterus + 0 Lythtypnus, and 15 Coryphopterus + 30 Lythrypnus), which were included both on reefs in exclosure cages and on reefs in open cages. Each of the ten combinations of predator exposure and goby density were included once in each of the three rows of reefs. Also, two completely uncaged reefs, to which no gobies were added, were included in each row. These uncaged reefs were used only to examine the responses of predators to caged versus uncaged reefs. 15 reefs were built within predator exclosure cages ( - P; Fig. Id), another 15 were inside predator-accessible open cages ( + P; Fig. le) and 6 were uncaged ( + P; Fig. lc). Treatments were assigned randomly within each row of the rubble reefs. Cages (complete and open) were cleaned at least once a week. All gobies were marked with acrylic tattoos, and after 3.5 weeks, those gobies remaining on the reefs were collected by divers using quinaldine and handnets. Survivorship (the number of marked fish recovered divided by the number of marked fish stocked) of the two species was compared over the 3.5-week period. Effects of predators on goby survivorship were tested with ANCOVA so that the effects of predators could be separated from those of competitors (intra- and interspecific) and spatial position (effects of reef row, a fixed categorical factor; and proximity to the mouth of the cove, a covariate). When the covariate did not explain a significant amount of the total variation in the experiment (P > 0.05) it was eliminated from the ANCOVA model. Because of this, the analysis for effects on Lythtypnus survivorship became an ANOVA. Also, to provide the strongest possible tests of predator effects, the factors reef row, Lythrypnus density and Coryphopterus density were eliminated from the statistical model and pooled with the error term when they explained an insignificant amount of the total variation (P > 0.25: Winer et al., 1991). To explore the effects of cages on the local abundance of predators of gobies, the number of potential predators present within 1 m of each replicate reef was recorded by divers when they first arrived at each reef. The mean of 11 observations (from 11 different days) was used as the estimate of predator abundance at each reef. Potential predators were divided into two groups: those which actively hunt gobies (the kelp and

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barred sand basses), and those which consume anesthetized gobies, but do not naturally pursue gobies (the wrasses Halichoeres semicinctus, Oxyjulis californicu, Semicossyphus pulcher) (pers. obs.). Differences among the three treatments in abundance of potential predators were tested for with Kruskal-Wallis non-parametric ANOVA because the data were not normally distributed (the distributions were strongly skewed). Since the shapes of the distributions were similar among treatments, nonparametric tests were appropriate.

3. Results 3.1. Experiment I: Standard and uncaged reefs

test for effects of predators:

Patterns of survivorship among treatments were and certain types of cage effects. For both species, predator exclosures, intermediate on partially caged completely uncaged reefs (Fig. 3). Although, for

cages,

“cage controls ”

consistent with both predator effects survivorship was highest on reefs in “cage control” reefs, and lowest on both species, survivorship on “cage

a) Lythrypnus

0.5, 0.4-

.:.:.:.: ...I... ........:.:. .::..:..T. .

0.3-

~~

.::::::::::y:::::::::: ..................,.,. j:j:j:i:j:i:l:l:l:l:j:i

,: :. T O.l.::. a . . . .r( cz 0 , ? .3 z o.2 _

iiiiiliii:“i,::.i:,: $:;:;,;$;.i:;,

I

b) Coryphoptems

tz

Exclosure Cage Control No Cage

Treatment Fig. 3. Mean survivorship of gobies on reefs with three different represent 1 standard error (SE), n = 3 for each treatment.

predator

exposure

regimes.

Error bars

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controls” was intermediate between exclosures and uncaged reefs, the effects of “cage controls” appeared to differ between the two species: survivorship of Lythrypnus on “cage controls” was very similar to that on uncaged reefs, in contrast, survivorship of Coryphopterus on the “cage controls” was much higher than on uncaged reefs, and, instead, was very similar to that on reefs in exclosure cages. The differences in survivorship among reef types were near statistical significance for both species (ANOVA: Coryphopterus, F,%, = 3.82, P = 0.085; Lythrypnus, F2.h = 3.53, P = 0.097). 3.2. Experiment of predators

2: Effects of cages: caged reefs versus framed

reqfs in the absence

Cages strongly affected Lythrypnus in a number of ways (Table 2). After 2 wk, more than twice as many Lythrypnus remained on caged reefs than on reefs surrounded only by frames, resulting in a significant difference in apparent survivorship between these two treatments (t-test, t = 5.02, df = 2, P = 0.037). Even though caged fish lived at higher densities, they grew significantly faster than uncaged (frame only) individuals (t-test, t = 6.74, df = 2, P = 0.021), more than quadrupling the growth of uncaged fish (Table 2). Movement among reefs was uncommon: only five fish switched reefs, one Coryphopterus (3.8% of those recaptured) and four Lythrypnus (5.6% of those recaptured). All five fish had moved from uncaged reefs onto reefs in an exclosure cage. The low rate of exchange among reefs indicates that any differences in growth caused by

Table 2 Responses

of Lythrypnus

A. Two-week

in the absence of predators

cages, open cages and frames

experiments Experiment

Apparent survivorship (fraction remaining) Growth (mm over 14 days) Foraging (bites min ’ ) Total aggression (chases min- ‘) Per capita aggression (chases fish- ’ min- ‘) Refuge use (% of time exposed)

B. One-day

to complete

2A

Experiment

3A

Cages

Frames

Cages

Open Cages

0.85+0.05

0.40?0.07”

0.46-tO.04

0.40%0.02

1.95_to.10 0.82?0.28 1.50~0.10

0.42-tO.20” 0.60?0.15 0.78+0.02”

2.lzL5t0.20 0.3 I to.03 0.34*0.03

2.21 10.29 0.44-to.07 0.2 I 1-0.04

0.059t0.001

0.067+0.013

0.02820.000

0.020 2 0.00s

7826

72~13

822 16

7026

experiments Experiment

Apparent survivorship (fraction remaining)

2B

Experiment

Cages

Frames

0.94+0.00

0.49+0.1

I”

All data are meanskstandard error from two replicate reefs. “ Significant difference, P < 0.05, between cages and frames. No differences were significant.

3B

Cages

Open Cages

0.97 20.03

0.95 +o.os

between cages and open cages

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the two caging treatments were probably not obscured by frequent movement among reefs. For Lyrhrypnus there were more aggressive acts on the higher density caged reefs than on the low density uncaged reefs (t-test, t = 7.03, df = 2, P = 0.020) but the per capita rate of aggression did not differ between caging treatments (r-test, t = - 0.60, df = 2, P = 0.60). Hence, it seems likely that differences in the total number of aggressive acts were caused by different densities of fish remaining in the two treatments and were not a direct result of cage effects. Foraging behavior (number of bites min-‘) and refuge use (fraction of total time spent perched on top of rocks, potentially exposed to predators) did not differ between treatments (r-tests, t = 0.72, df = 2, P = 0.55, and t = 0.41, df = 2, P = 0.72, respectively). Cages had no detectable effects on behavior, growth, or survivorship of Coryphopterus (Table 3). The one-day experiment (Experiment 2B) revealed that differences in the densities of Lythtypnus between caged and uncaged reefs developed rapidly. Within 24 h about half as many Lythrypnus remained on uncaged (framed) reefs as on caged reefs (Table 2B), and like the long term experiment, these treatments differed significantly in apparent survivorship (t-test, t = - 4.82, df = 2, P = 0.040). Since the reefs were not exposed to any predators, this result indicates that differences in density between the caging treatments are likely the result of relatively rapid behavioral decisions by gobies to abandon reefs surrounded only by frames. For all of the experiments conducted inside the large predator exclosure, many of the gobies that abandoned the experimental reefs were found at the bottom edge of the net predator barrier. 3.3. Experiment 3: Tests for differences cages in the absence of predators

between effects of exclosure

cages and open

Open cages (Fig. le) and complete exclosure cages (Fig. Id) appeared to have similar effects on Lythrypnus (Table 2). In both the 2-week and l-day experiments the fraction of Lythrypnus that remained on reefs did not differ significantly between the two cage types (t-tests, t = 0.15, df = 2, P = 0.90, and t = 1.34, df = 2, P = 0.31, respectively). Further, no differences in growth or behavior were detected. These results indicate that these two cage designs may be used to explore the effects of predators on Lythrypnus without confounding predator effects with effects of cages on the prey.

Table 3 Responses

of Coryphopterus

on caged and uncaged (frame only) reefs in the absence of predators (Experiment

2A)

Apparent survivorship (fraction remaining) Growth (mm over 14 days) Foraging (bites min-‘) Total aggression (chases min- ‘) Per capita aggression (chases fish-’ min-‘) Refuge use (% of time exposed to predators) All data are meanskstandard error statistically significant (P > 0.05)

from

two replicate

Cages

Frames

0.60+0.10 4.38kO.18 0.48-tO.28 0.3o_fo.15 0.02220.012 18214

0.65 kO.05 5.20k0.45 0.32+0.08 0.35 to. 15 0.032+0.014 77212

reefs.

No differences

between

treatments

were

M.A. Steele I J. Exp. Mar. Biol. Ecol. 198 (1996) 249-267

261

0.41

*

0.3 .tia c z .d9

i2 s

0.”

0.I 0

T

’

I

“,

Lythrypnus

Coryphopterus

Fig. 4. Mean survivorship on reefs exposed to predators (open cages) and reefs not exposed to predators (exclosures). Error bars represent I SE. For Lythrypnus, n = 9 for each bar, and for Coryphopterus, n = 6 for each bar. An asterisk indicates that means differed significantly (P < 0.05) between exclosure versus open cages.

3.4.

Experiment

4: Effects of predators

on Lythrypnus

and Coryphopterus

greatly reduced survivorship of Lythrypnus, but they did not affect Survivorship of Lythrypnus on reefs in exclosure cages ( - P) was about twice as high as on reefs in open cages ( + P, Fig. 4). This difference was highly significant: ANOVA, F,, , 6 = 10.4, P = 0.0005. In contrast, survivorship of Coryphopterus in exclosure cages was only = 14% greater than that in open cages, not a significant difference (ANCOVA, F,., = 0.61, P = 0.463, Fig. 4). Known predators of gobies (the basses, Paralabrax spp.) were more abundant around complete exclosures than around open cages or reefs with no structures (Kruskal-Wallis test, P = 0.008, Fig. 5a). Although approximately twice as many of these predators were found near partially caged reefs as near uncaged reefs, this difference was not statistically significant (Mann-Whitney U-test, P = 0.38). Abundances of other potential predators (wrasses) did not differ significantly among the three reef types (KruskalWallis test, P = 0.68, Fig. 5b). Predators

Coryphopterus:

4. Discussion 4.1. Importance

of direct tests for cage artifacts

Predators have long been thought to play an important role in structuring reef fish populations (Smith, 1978; Talbot et al., 1978). However, surprisingly few studies (e.g., Anderson, 1993; Caley, 1993; Carr and Hixon, 1995) have demonstrated predator effects on reef fish population density without confounding predator effects with cage or shelter effects (e.g., Shulman, 1984, Shulman, 1985; Doherty and Sale, 1985; Behrents, 1987;

262

M.A. Stedr

I .I. Exp. Mar. Bid.

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19X (19%) 249-267

a) Paralabrax spp.

0.8

b) Other Potential Predators 0.8-

0.6-

a

1 . ../..../.......... ................i..... ii......... ,.,.,.,.,. ..............

...I... .....A.... .................

0.4-

O.‘,J

a

gggj:j, .........../..../// ..................

.............\/..\ ..l/..\.. . .. ” .,”

;

_T_ :

‘,

Exclosure

Open Cage

No Cage

Treatment Fig. 5. Mean abundance of potential goby predators at reefs enclosed in complete cages and open cages, and at reefs with no structures. Puralabrax species included P. clathratus and f. nebulifer, which are known to prey upon the gobies. Other potential predators were Semicossyphus pulcher, Hulichoeres semicinctus and Oxyjuli.s californica. Error bars represent 1 SE. n = 15, 15, and 6 for exclosures, open cages, and uncaged reefs respectively. Means sharing a common letter do not differ significantly, P < 0.05 (Mann-Whitney U-test).

Hixon and Beets, 1989, Hixon and Beets, 1993; Carr, 1991; Connell, 1994). Demonstrating that the means of manipulating predation intensity (i.e., cages or shelter) is not the cause of purported predator effects is essential and requires that direct tests of the potential artifacts be made. For example, by conducting direct tests of cage effects in the absence of predators, it was found that one species of temperate zone reef fish (Lythrypn~s dalli) was strongly affected by cages, while another species (Cotyphopterus nicholsii) was not. The differences between caged and uncaged (framed) reefs were exactly what would be expected if predators had strong effects on Lythrypnus: decreased densities of fish, lower growth, and less activity on uncaged reefs. Therefore, using these two treatments to assess the effects of predators on this species would result in hopelessly confounded results, which is what was found in a test of predator effects using the standard, cage, “cage control”, and no cage design (Experiment 1). In this case, differences among treatments were consistent with both predator and cage effects, for both species. These results would suggest that, ideally, using cages or shelter to manipulate predation

M.A. Steele I J. Exp. Mar. Biol. Ecol. 198 (1996) 249-267

263

pressure should be avoided, and for a limited number of very sedentary piscivorous fishes, this is a promising and feasible approach (see Can and Hixon, 1995). However, many predators of fishes are highly mobile, and hence, manipulating their presence will probably require the use of cages. In these cases, appropriate tests for cage effects will need to be made. 4.2. Potential

causes of “cage effects ”

It is unclear what aspects of cages caused Lythrypnus to do better on caged reefs relative to uncaged (framed) reefs, in the absence of predators. Differences in density between the two treatments developed rapidly (within 24 h), suggesting that the fish preferred caged reefs and responded behaviorally. The most commonly noted abiotic changes wrought by underwater cages are reduced water flow and shading within cages (e.g., Vimstein, 1977, Virnstein, 1978; Peterson, 1979; Hurlberg and Oliver, 1980; Schmidt and Warner, 1984; Hayworth and Quinn, 1990; Peckarsky and Penton, 1990). Often it is thought that prey do not respond directly to these abiotic changes but instead respond to decreased plant production, lowered abundance of planktonic food, or increased sedimentation brought about by shading and reduced water flow (e.g., Hurlberg and Oliver, 1980; Peckarsky and Penton, 1990; Kennelly, 1991). It is not likely that Lythrypnus responded to these sorts of changes; differences in algal abundance and sedimentation were not apparent (and were very unlikely to develop within 24 h), and reduced abundance of planktonic food in caged areas would have caused caged fish to do more poorly than their uncaged counterparts, the opposite of the observed pattern. Another change that has been observed in caged areas is an increase in macroalgae caused by the unintentional exclusion of herbivores (Doherty and Sale, 1985). This. too, cannot be the cause of the detected cage effects because of the relatively long time required for such a difference to develop. One of the most obvious abiotic changes caused by cages is increased vertical relief from the cage itself. Midwater fishes have been observed to orient to this vertical structure (Doherty and Sale, 1985) but the benthic Lythrypnus were never observed using the vertical cage structure as shelter. It is suspected that Lythrypnus responded directly to differences in light intensity between caged and uncaged reefs. Light level may be used as a cue for assessing habitat quality: Lythrypnus grow at faster rates in deeper (darker) areas (Steele, 1995) and fish density declines from moderately deep (= 25 m) to shallow sites (M.A. Steele, unpublished), suggesting that shallow, brightly lit, areas may represent poor habitat for this species. Schmidt and Warner (1984) found that ascidians used light intensity as a cue for settlement and thus settled at higher densities in cages. Light intensity may be a commonly used behavioral cue, and hence, shading by cages may directly cause “cage effects” in a variety of animal taxa. 4.3. Utility of “cage controls” To assess the potential for cage artifacts, ecologists sometimes directly measure the effects of cages on parameters that are believed to affect prey organisms, for example, algal growth (Hurlberg and Oliver, 1980) sedimentation (Peckarsky and Penton, 1990)

264

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I J. Exp. Mar.

Bid.

Ed.

I!% (1996)

24%,767

and plankton abundance (Anderson, 1993). However, even when these parameters differ between caged and uncaged areas, and the differences are associated with patterns of prey abundance, this does not establish that “cage effects”, instead of predation, are responsible for differences in prey abundance. Moreover, finding no difference in these parameters between “cage controls” and cages does not prove that artifacts of caging do not exist; prey may respond to some other cage-induced change. Use of many different “cage controls” may help to elucidate the factors affecting prey abundance (e.g., Hurlberg and Oliver, 1980; Schmidt and Warner, 1984), but these “control” treatments will likely reduce access of prey to some predators, confusing the issue. For these reasons, direct tests of cage artifacts, in the absence of predators, are probably the only reliable means of exploring cage effects on prey. By using direct tests, it was demonstrated that there were no differences between the effects on prey by devices that excluded predators (cages) and others that allowed predators access to prey (open cages). This meant that tests for predator effects using these devices would not be confounded with “cage effects.” The subsequent experiment using these predator manipulation treatments indicated that predators greatly reduced survivorship of Lythrypnus. Survivorship of Coryphopterus was not affected by predators. This result is problematic and it highlights an interpretation problem inherent in using partial cages as a predator-exposed treatment: predator effects will likely be underestimated because partial cages often lower the accessibility of prey to predators. In the absence of predators, cages were found to have no effects on Coryphopterus (Experiment 2A). Since there were no cage effects on this species, the difference in survivorship between caged reefs and uncaged reefs, in the presence of predators (Experiment l), should be a reliable estimate of the effect of predation on Coryphopterus. Apparently, predators reduced survivorship by = 75%. In order for there to have been no difference in survivorship of Coryphopterus between complete and “open cages”, the ability of predators to consume this species must have been greatly reduced by partial cages (see Fig. 3b and Fig. 5). It is likely that the effects of predators on Lythrypnus were somewhat reduced by partial cages too. Thus, although differences in survival between reefs in exclosure cages and in “open cages” can clearly be attributed to the effects of predators, a lack of difference between these two treatments cannot be used as strong evidence that predators had no effects on their prey. This is because predator efficacy may be reduced by partial cages. To further complicate the issue of determining the actual magnitude of predator effects under natural conditions, cages may also affect the distribution and abundance of predators. For example, predators may aggregate to caged and partially caged areas due to the presence of the structures (Arntz, 1977; Vimstein, 1978; Carr, 199 1; this study). When predators aggregate at partial cages, the magnitude of predator effects will generally be overestimated if caged and partially caged areas are compared (Dayton and Oliver, 1980; Underwood and Denley, 1984), provided that the partial cages do not decrease the efficacy of the aggregated predators. Alternately, predators may avoid partially caged areas, in which case, comparing partially caged areas to areas in exclosure cages will underestimate the true magnitude of predator effects. Another problem associated with caging studies is that small non-target predators sometimes take

M.A. Steele / .I. Exp. Mar. Biol. Ecol. 198 (1996) 249-267

2hS

up residence in exclosure cages (e.g., Arntz, 1977; Vimstein, 1978) causing the overall effect of predation to be underestimated (Dayton and Oliver, 1980; Choat, 1982). Because both predator and prey behavior may be affected by cages and partial cages, careful documentation of predator and prey behavior at caged, partially caged, and uncaged areas is essential to interpret accurately the results of caging studies. Detailed observations of predator-prey interactions under natural conditions (no cages) may be useful in determining whether prey respond to predators in the same ways and at the same frequencies noted in cage studies. 4.4. Effects of predators

on reef fishes

This study provides some of the first direct experimental evidence that predators have strong effects on survivorship of reef fishes. It is not surprising that predators drastically reduced the abundance of both Lythrypnus and Coryphopterus, since predators have strong effects on the abundance of many taxa (reviewed in Sih et al., 1985), and there exists considerable circumstantial evidence that is suggestive of important effects by predators on abundance of reef fishes (reviewed in Hixon, 1991), coupled with a small, but growing, body of direct experimental evidence for effects by predators on reef fish abundance (Anderson, 1993; Caley, 1993; Carr and Hixon, 1995). Since cage effects on Lythrypnus were tested for directly, and none were found when comparing exclosure and open cages, the reduced survivorship of this species was confidently attributed to effects of predators. However, the magnitude of the detected predator effect may not reliably estimate the magnitude of the natural effect of predators on this goby, because partial cages may have affected the abundance or behavior of the predators. Because of these sorts of possible cage effects on predators, the use of partial cages should be avoided where possible. A challenge for marine ecologists is to determine the magnitude of natural predator effects on reef fish population abundances. For species that are affected by transient predators, whose densities cannot be manipulated by removal, caging studies are currently the only effective technique for exploring the effects of predators. For caging studies to provide the most accurate estimates of natural predator effects, cages that are essentially invisible (possibly achieved by using clear, large mesh netting material), and therefore do not affect prey or predator behavior, must be developed. By using such techniques, we may begin to appreciate the true importance of predation as source of post-settlement mortality in reef fishes. In conclusion, often it is not feasible to manipulate predator densities by any means other than by using exclusion devices (usually some sort of cage). This commonly used approach suffers numerous problems of interpretation, not the least of which is deciphering the importance of predation when cages affect prey. This study demonstrated that cages can strongly affect the behavior and subsequenr performance of organisms living in predator exclusions. The observed effects were unexpected and would completely confound any attempt to determine the effects of predators. However. this study also demonstrated that by directly testing for effects of cages on target prey, treatments can be developed that do not confound cage artifacts with predator effects. Hence, detected effects can then be reliably attributed to predation. Observing the

266

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198 (199b) 249-267

behavior of predators and prey, both in manipulated areas and under natural conditions, will aid in the interpretation of results from caging studies. Until some better technique is developed, caging studies will remain one of the most commonly used means of documenting the effects of predators and with some effort and ingenuity, the results of such studies will be more readily interpreted.

Acknowledgments S. Anderson, M. Carr, G. Catalano, B. Fredericks, M. Hearne, T. Henry and B. Sabado provided assistance with the experiments. T. Anderson, M. Carr, S. Holbrook and R. Schmitt had useful ideas and suggestions. As always, l? Raimondi gave advice on some statistical analyses. Helpful comments on various drafts of this paper came from M. Cam, G. Forrester, S. Holbrook and B. Warner. Financial and intellectual support came from my advisor S. Holbrook. Thanks to D. Bocskai for being understanding. The gang at Wrigley Marine Science Center helped with logistics. Funding came from NSF grant OCE-91-82941 to R.J. Schmitt and S.J. Holbrook, Sigma Xi and Lemer-Gray grants to the author, and additional financial support from fellowships from the University of California at Santa Barbara (Regents and Continuing Graduate Student Fellowships), scholarships from the International Women’s Fishing Association and from the R. and S. Steele fund for underfunded graduate students. This is Contribution Number 159 from the Wrigley Marine Science Center at Catalina.

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