Foraging habitats and interspecies interactions of the striped red goatfish, Mullus surmuletus

Jessica R. Hanaway-Moore and Gabrielle R. Keeler University of California, Santa Cruz Department of Ecology and Evolution Corsica Field Quarter, Fall 2012

Keywords goatfish, habitat specialization, foraging behavior, interspecies interactions, community ecology

Abstract

With this study, we aimed to determine whether M. surmuletus exhibit specific foraging habitats and to describe the relationship between M. surmuletus and other fish species. We used bite rate as a proxy to determine costs and benefits. We found that M. surmuletus is a habitat specialist and exhibits ontogenetic shifts in habitat utilization. Additionally, M. surmuletus acts as a nuclear species in foraging associations and positively affects the feeding rate of follower fishes. We also identified a relationship between follower species composition and foraging habitat.

Introduction

The striped red goatfish, Mullus surmuletus, are benthic carnivores distributed along the eastern Atlantic and throughout the Mediterranean Sea. Adults can be found in depths greater than 400m, while juveniles tend to reside in shallower waters (Machias et al. 1998). In the Mediterranean Sea, M. surmuletus is a commercially important food fish and has been subjected to intense exploitation, mostly via trawling, with young fish being subjected to the greatest fishing pressure. (Tserpes et al. 2002). Studies have found ontogenetic diet shifts of trawled goatfish populations (Kolasinski et al. 2009; Chérif et al. 2011; Bautista-Vega et al. 2008; Labropoulou & Eleftheriou 1997; Labropoulou et al. 1997), but they have not looked specifically at those living in shallow water, nor have they looked at foraging behavior. Likewise, few studies have examined habitat utilization of goatfish and none have studied M. surmuletus. Understanding juvenile habitat selection and usage is critical for designing effective management strategies because healthy juvenile populations are important for maintaining adult goatfish populations. Recognizing community interactions is also fundamental to the persistence and stability of natural populations. The linkage between species is the foundation of community infrastructure and can be a vital component in the rise or fall of populations. Other species of goatfish are known to participate in what are called nuclear-follower foraging associations (Sazima et al. 2007). Nuclear fish form the core of a foraging association, while follower fish accompany these fish during foraging or while travelling between foraging habitats. Past studies on nuclear-follower foraging describe the composition of these associations (Sazima et al. 2007; Lukoschek & McCormick 2002), but do not investigate possible benefits of associating. Such relationships are difficult to quantify and ours is the first study to use feeding rate as a proxy for overall benefit of nuclear-follower foraging associations. Using observational data, we addressed the following questions: (1) How does M. surmuletus interact with their foraging habitat? (2) What is the relationship between M. surmuletus and their follower fish? (3) Is there a correlation between follower fish and M. surmuletus foraging habitat?

Methods

Data Collection

We observed the feeding habit and relationship of Mullus surmuletus with other Mediterranean fishes in different substrate types along the northwestern coast of Corsica, France at Station de Recherche Océanographiques et sous-marines (STARESO). This area is characterized by large, continuous Posidonia oceanica meadows as well as patches of sandy and rocky bottoms. The study site did not exceed 12 m depth and the mean water temperature was 21°C. We collected observations in daylight hours during October 2012 when ocean conditions were calm with minimal swell and wave action. To assess foraging habitat use, we took uniform point contact (UPC) data in sites where we observed M. surmuletus foraging during preliminary observations. We completed twenty 30x2m transects at depths ranging from 4 to 8 m with headings running near parallel to the adjacent shoreline. We assigned the habitat to six substrate categories: (1) Turf algae: foliose green algae, brown algae or erect coralline algae covering boulders and bedrock, (2) Posidonia oceanica: dominant seagrass species found in large meadows or small patches, (3) Sand: sediment less than 1 cm, (4) Cobble: sediment between 1 to 10 cm, not covered by any turf algae, (5) Dead P. oceanica: sites covered by thick layers of necrotic seagrass, (6) Other: any other substrate type, including encrusting algae, sessile invertebrates, and bare rocks larger than 10 cm. To assess the foraging habits of M. surmuletus, we opportunistically observed individuals within our study area while on SCUBA. To avoid depth bias, we conducted meandering search patterns that encompassed a wide depth range where M. surmuletus could be found. We only took data while swimming away from STARESO (north or south) to avoid repetitive observations of individual M. surmuletus and to avoid observational interference, which may have arisen from disturbances created by data collectors. Likewise, we did not take observations more than once a day for a given heading. When a M. surmuletus was found, we recorded the depth and visually estimated their lengths using marked dive slates as size references. We then observed the foraging strategies of each goatfish for two minutes, taking data on the number of feeding instances and noting the habitat of each feeding instance. A feeding instance began when the barbels were deployed and ended when the goatfish’s snout was lifted from its downward feeding position. We used the number of feeding instances divided by time observed as a proxy for an individual’s bite rate. In addition, we noted any fishes associating with M. surmuletus during these two-minute observations. The fish species were identified and the number present was recorded. We defined an associate species as any fish that came within half a meter of the goatfish during feeding instances. To further investigate the relationship between M. surmuletus and associate fishes, we then conducted a new set of opportunistic surveys focused on the species found most often with the goatfish in the previous search. We observed each associate fish for a maximum of two minutes. During this time, we recorded the amount of time (in seconds) an associate spent alone, time with a M. surmuletus, and time with any other fish species. Again, we used feeding instances over time as a proxy for bite rate of associate fishes.

Data Analysis

We began our analysis of habitat use by combining our own UPC data with harbor UPC data collected by Tristan McHugh and Kristen Elsmore (2012) to calculate the proportion of available foraging habitats. We considered the number of goatfish bites observed over a given foraging habitat to be representative of the amount of time the goatfish spent over a specific foraging habitat. We compared the available habitat to the observed foraging habitat by conducting a Pearson chi-squared analysis. In order to determine a relationship between goatfish size and foraging habitat, we separated goatfish individuals into two categories, small (<15cm) and large (>15cm), and did a PERMANOVA analysis (in PRIMER). We assessed the question of specific follower species by comparing the proportion of fish species present at the study site to the proportion of follower species we observed with goatfish during feeding instances. We used the available fish data from fish transects done for other similar projects (Bernardi 2010). We compared the available fish species to the actual follower fish species by conducting a Pearson chi-squared analysis. Using linear regression, we tested the hypothesis that the relationship between M. surmuletus and their follower fish was commensal by first comparing goatfish feeding rate and total goatfish associates. To examine differences in feeding rates of follower species when alone and with M. surmuletus, we ran an ANOVA in JMP. We also chose to compare the community composition of follower species with goatfish foraging habitat. The community composition refers to the unique makeup of follower fish that were found with an individual goatfish. We used PERMANOVA analyses (in PRIMER) to determine a correlation between these two factors. We also conducted a RELATE test (in PRIMER) to show the strength of the relationship between follower species composition and foraging site.

Results

A total of 69 goatfish and 213 follower individuals were observed for a total of 172 hours and 35 minutes. Presence of an observer did not appear to affect the behavior of most study fish. During a few observation sessions, individual Coris julis switched focus from foraging to examining the observer, in which case a new individual was chosen for observation. M. surmuletus size ranged from 5cm to 21.5cm. Goatfish smaller than 15cm were considered small and goatfish greater than or equal to 15cm were considered large. Follower species size was not recorded.

Foraging Habitat

The two most abundant habitat types surveyed were turf algae (49%) and Posidonia oceanica (15%). All other habitat types accounted for less than 10% each of the remaining habitat. M. surmuletus foraged on turf algae approximately 78% of the time, sand 12%, cobble 6%, and dead Posidonia 4%. We did not observe M. surmuletus foraging in P. oceanica or “other” substrates. Foraging habitat used by M. surmuletus is significantly different from available habitat in the study site (χ² = 311.014, p < 0.0001, Figure 1). Small goatfish exhibited different foraging tendencies compared to large goatfish (p = 0.001). Large goatfish foraged on a broad range of habitats while small goatfish were generally restricted to foraging in turf algae (Figure 2).

Follower Species

Of the 21 species of fish present at the study site, four species (Coris julis, Diplodus vulgaris, Symphodus rostratus, and Symphodus tinca) associated more frequently with striped red goatfish disproportionate to their relative abundance (p < 0.0001, Figure 3). The presence of follower species had no effect on the feeding rate of M. surmuletus (p = 0.984). However, feeding rate of follower species increased when they foraged with the goatfish versus when they foraged alone (Figure 4). In all cases, follower feeding rate was significantly higher when a follower foraged with a goatfish than when foraging alone (p = 0.0163).

Foraging habitat and follower fish

There is a strong relationship between species composition of follower groups and foraging habitat (Rho = 0.936, p = 0.001). The species composition of followers with goatfish foraging on turf is different than the composition of followers with goatfish foraging on non-turf habitats (Figure 5).

Discussion

Foraging habitat

Our results indicate that juvenile M. surmuletus are specialists with regards to foraging habitat utilization. Further, M. surmuletus exhibit an ontogenetic shift in degree of specialization, tending towards a more generalist utilization of available foraging habitats. Such trends have been studied in other fish families (Jones 1984, Ajemian & Powers 2012, Clark & Russ 2012) and may be due to behavioral, ecological, or developmental patterns. Jones (1984) found that early life stages of wrasse were more aggregated than adults, which were more randomly dispersed. While our study does not examine wrasses or adult M. surmuletus, we are inclined to believe this pattern is the same in our study system. Previous studies have recorded ontogenetic shifts in diet of M. surmuletus and other species of goatfish (Gharbi & Ktari 1979; Golani & Galil 1991; N'Da 1992; Labropoulou & Eleftheriou 1997; Labropoulou et al. 1997; Machias & Labropoulou 2002; Bautista-Vega et al. 2008; Kolasinski et al. 2009; Chérif et al. 2011), which may be directly related to prey composition in each foraging habitat. The smallest M. surmuletus may be foraging most often in turf algae because their preferred prey is most abundant in that habitat, but further investigation is needed to determine whether there are differences in prey composition between foraging habitats. Another explanation of foraging habitat shift is barbel development rate. Goatfish barbels develop rapidly from the moment of settlement and continue to develop as goatfish grow (Uiblein 1991, McCormick 1993). However, our study does not investigate the ability of smaller M. surmuletus to forage in varying habitats and additional study is needed to determine if they are restricted to turf algae by developmental limitations.

Nuclear-follower foraging associations

We found that specific fish species follow M. surmuletus during foraging bouts, which is consistent with the findings of Strand (1988). Feeding associations, such as these, have been recognized as an important aspect of community structure in tropical systems (Sazima et al. 2007). It has been suggested that follower species may benefit from foraging associations through ease of foraging and predator avoidance (Lukoschek & McCormick 2000). Nuclear fish stir up prey items making them easier for follower fishes to catch or locate (Kushlan 1978). Thus, follower fishes expend less energy while foraging with a nuclear species than while foraging alone (reviewed in Lukoschek & McCormick 2000). Using bite rate as a quantitative measurement of cost/benefit to M. surmuletus and their follower fish, our results indicate that this nuclear-follower foraging association is commensal (0/+). Bite rate of M. surmuletus is unaffected by follower abundance, while the bite rate of all follower species is positively affected while foraging with M. surmuletus. Our data are consistent with Sanderson (1987) in which a follower labrid increased 'strike rate' when associating with goatfish. Other studies have found that there is overlap between nuclear species and follower species diet (Strand 1988), however, our study does not address diet of goatfish or follower fish and more data would be needed to determine this pattern in M. surmuletus. We did not observe any aggression from nuclear fish towards follower fish, so we believe that competition for food between the two is unlikely.

Follower fish and foraging habitat

To our knowledge, this study is the first to identify a relationship between follower fish species composition and nuclear foraging habitat. It is likely that this relationship is driven more by the fish species composition over each habitat type than by the presence of M. surmuletus. A study of nuclear-follower foraging associations in the Gulf of California by Strand (1988) identified 21 different nuclear species, most of which cause substrate disturbances while foraging. Sazima et al. (2007) suggests that follower species are attracted to these foraging disturbances rather than particular nuclear species. Additionally, Krajewski (2009) experimentally found that follower species are more likely to aggregate around substrate disturbances than potential nuclear species. If we were to examine habitat preference of follower species, we may find a similar follower composition relationship with habitat type irrespective of nuclear species.

Acknowledgements

We thank our professors Pete Raimondi and Giacomo Bernardi for their patience with all of our questions, Gimmy O’Dongo and Kristen de Nesnera for their insightful and constructive criticism. The entire staff at STARESO, especially Richard for feeding us. And thanks to our Bioe 159 field colleagues who helped with data collection and kept us sane throughout the storm.

References

Ajemain MJ, Powers SP (2012) Habitat-specific feeding by cownose rays (Rhinoptera bonasus) in the northern Gulf of Mexico. Environmental Biology of Fish, 95: 79-97 Bautista-Vega AA, Letourneur Y, Harmelin-Vivien M, Salen-Picar C (2008) Difference in diet and size-related trophic level in two sympatric fish species, the red mullets Mullus barbatus and Mullus surmuletus , in the Gulf of Lions (north-west Mediterranean Sea). Journal of Fish Biology, 73(10): 2402–2420. Chérif M, Ben Amor MM, Selmi S, Gharbi H, Missaoui H, Capape C (2011) Food and feeding habits of the red mullet, Mullus barbatus (Actinopterygii: Perciformes: Mullidae), off the northern Tunisian coast (central Mediterranean). Acta Ichthyologica Et Piscatoria, 41(2): 109–116. Clark NJ, Russ GR (2012) Ontogenetic shifts in the habitat associations of butterflyfishes (F. Chaetodontidae). Environmental Biology of Fish, 94: 579-590 Kolasinski J, Frouin P, Sallon A, Rogers K, Bruggemann HJ (2009) Feeding ecology and ontogenetic dietary shift of yellowstripe goatfish Mulloidichthys flavolineatus (Mullidae) at Reunion Island, SW Indian Ocean. Marine Ecology Progress Series, 386: 181–195. Golani D, Galil B (1991) Trophic relationships of colonizing and indigenous goatfishes (Mullidae) in the eastern Mediterranean with special emphasis on decapod crustaceans. Hydrobiologia, 218: 27-33 Gosline, W. A. 1984. Structure, Function, and Ecology in the Goatfishes (Family Mullidae). Pacific Science 38(4): 312-323 Gotceitas V, Fraser S, Brown JA (1995). Habitat use by Atlantic cod (Gadus morhua) in the presence of an actively foraging and non-foraging predator. Marine Biology, 123: 421-430 Jones GP (1984) The influence of habitat and behavioral interactions on the local distribution of the wrasse, Pseudolabrus celidotus. Environmental Biology of Fish 10(½): 42-58 Labropoulou M, Machias A, Tsimenides N, Eleftheriou A (1997) Feeding habits and ontogenetic diet shift of the striped red mullet, Mullus surmuletus Linnaeus, 1758. Fisheries Research, 31(3): 257–267. Labropoulou M, Eleftheriou A (1997) The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. Journal of Fish Biology, 50(2): 324–340. Lukoschek V, McCormick M (2000) A review of multi-species foraging associations in fishes and their ecological significance. Proceedings V, International Coral Reef Symposium. Bali, Indonesia, 1: 23-27 Machias A, Somarakis S, Tsimenides N (1998) Bathymetric distribution and movements of red mullet Mullus surmuletus. Marine Ecology Progress Series, 166: 247–257. Machias A, Labropoulou M (2002) Intra-specific variation in resource use by red mullet, Mullus barbatus. Estuarine, Coastal and Shelf Science 55: 565-578 McCormick MJ (1993) Development and changes at settlement in the barbel structure of the reef fish, Upeneus tragula (Mullidae). Environmental Society of Fishes, 37: 269-282 McCormick M (1995) Fish feeding on mobile benthic invertebrates: influence of spatial variability in habitat associations. Marine Biology, 121: 627-637 Reñones O, Massutí E, Morales-Nin B (1995) Life history of the red mullet Mullus surmuletus from the bottom trawled fishery off the Island of Majorca (north-west Mediterranean). Marine Biology, 123: 411-419 Sazima C, Krajewski JP, Bonaldo RM, Guimarães PR Jr (2006) The goatfish Pseudupeneus maculatus and its follower fishes at an oceanic island in the tropical west Atlantic. Journal of Fish Biology, 69(3): 883–891. Sazima C, Krajewski JP, Bonaldo RM, Sazima I(2007) Nuclear-follower foraging associations of reef fishes and other animals at an oceanic archipelago. Environmental Biology of Fishes, 80(4): 351–361. Strand S (1988) Interspecific foraging associations among Gulf of California reef fishes. Copeia, 2: 351-357 Tserpes G, Fiorentino F, Levi D, Cau A, Murenu M, Zamboni A, Papaconstantinou C (2002) Distribution of Mullus barbatus and M. surmuletus (Osteichthyes: Perciformes) in the Mediterranean continental shelf: implications for management. Scientia Marina, 66(2): 39- 54 Uiblein F (1991) Ontogenetic shifts in resource use and shoaling tendency related to body size in Red Sea goatfish (Parupeneus forsskali, Mullidae). Marine Ecology, 12(2): 153-161

Figures

80% Foraging Habitat Available Habitat

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0% Cobble Dead Posidonia Other Posidonia Sand Turf Habitat Types

Figure 1. Percent composition of available habitat (red) in the study site compared to percentage of each habitat type utilized by goatfish during foraging (blue).

Figure 2. Differences in habitat utilization between small (blue) and large (red) M. surmuletus. Small goatfish were found most often foraging in turf algae and large goatfish were more evenly distributed throughout the four types of foraging habitat.

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Fish Species Figure 3. Percent abundance of fish species present at the study site compared with percent abundance of fish species observed with M. surmuletus. Blue bars represent fishes observed during surveys of the study site. Red bars represent fishes observed participating in nuclear-follower foraging associations with M. surmuletus. We did not have enough data on D. annularis, S. tinca, and follower M. surmuletus to include these three species in further statistical analyses.

0.12 Alone With Mullus

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0.00 C. julis D. vulgaris S. rostratus S. tinca Fish Species Figure 4. Feeding rates of follower species while foraging with and without M. surmuletus. Blue bars represent bite rates of follower species while foraging alone. Red bars represent bite rates of follower species while participating in nuclear-follower foraging associations.

Figure 5 Differences in follower species composition between goatfish foraging on turf algae (blue) and not on turf algae (red). The group columns show the average abundance of the respective follower species within their group. When goatfish were found foraging on turf they were more likely to be followed by C. julis than any other followers. When goatfish were found foraging on non-turf habitats, they were more likely to be followed by C. julis and S. tinca.