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Prey-size selectivity in the bivalve Chione in the Florida Pliocene-Pleistocene :
b a re-evaluation
h [electronic resource] /
by Shubhabrata Paul.
[Tampa, Fla] :
University of South Florida,
Title from PDF of title page.
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Thesis (M.S.)--University of South Florida, 2008.
Includes bibliographical references.
Text (Electronic thesis) in PDF format.
ABSTRACT: Previous study of drilling predation on the bivalve Chione during the late Neogene of Florida suggested that prey-size selectivity of predators was disrupted by species turnover and morphological change within the prey genus. More recent experimental work, however, showed that at least some of these changes can be attributed to the confounding effects of facies shifts between naticid-dominated, muricid-dominated, and mixed predator assemblages. As muricids have the most abundant and continuous fossil record and are most responsible for predation on the Chione bivalve in modern benthic ecosystems of Florida, we use new criteria to isolate the muricid component of the Chione drillhole record and analyze the history of this type of predator independently. Our analysis, based on drilled Chione from four Plio-Pleistocene formations in Florida, does not support the previous scenario of disruption at the end of the Pliocene followed by predator recovery.Rather, selected prey size has steadily increased since the middle Pliocene, although the stereotypy of prey-size selection behaviors has decreased. In order to explain this trend, I performed a series of statistical analyses to explore factors most likely to have influenced muricid prey-size stereotypy. The timing of Species turnover within the prey lineage or change in prey phenotype does not correlate with the timing of changes in prey-size stereotypy and, therefore, cannot explain the observed changes in muricid behavior. Presence of secondary predators may also influence predator-prey interactions, because predators forage sub-optimally to ensure greater safety in the presence of enemies. Results indicate that secondary predation pressure decreased at the Caloosahatchee-Bermont boundary without any evident change in muricid prey-size stereotypy and hence refute the hypothesis that secondary predation induced sub-optimal foraging.A third factor tested is prey density, which plays a major role in predator-prey interactions in other systems by thwarting a predator's ability to single out the preferred individual prey. Increased Chione prey density correlates with and provides support for increased confusion among the muricid predators and hence driving the increased sub-optimal behavior reflected by the increased variability in prey-size selection. This is the first time prey density effect has been considered and its importance here over all other factors suggests that it may be a critical factor in short- and long-term predator behavior trends in fossil record.
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Advisor: Gregory S. Herbert, Ph.D.
t USF Electronic Theses and Dissertations.
Prey-size selectivity in the bivalve Chione in the Florida Pliocene-Pleistocene: A reevaluation by Shubhabrata Paul A thesis submitted in partial fulfillment of the requirements for the degree of Masters of Science Department of Geology College of Arts and Science University of South Florida Major Professor: Gregory S. Herbert, Ph. D. Peter J. Harries, Ph. D. Gregory P. Dietl, Ph. D. Date of Approval: November 6, 2008 Keywords: Chione extinction, gastropod, prey-density, stereotypy Copyright 2008, Shubhabrata Paul
Dedication This thesis is dedicated to my dear sister, Sampi. Although she is younger than me, she has taught me how to stand tall in difficult times. She has always been a great source of inspiration and motivation.
Acknowledgements I would like to express my deep and sincere gratitude to my supervisor, Dr. Gregory S. Herbert for his enthusiasm, his insp iration, his great effort s to explain things clearly and his patience to improve my writing skill. Throughout my thesis-writing period, he provided encouragement, sound advice, good teaching, lots of good ideas and some crazy songs. I would like to thank Dr. Peter J. Harries a nd Dr. Gregory P. Dietl for their critical opinion in preparing this thesis. I am thankful to my student colleagues for providing a stimulating and fun environment. I am especially grateful to Je nnifer Sliko and Julie McKnight. This thesis would not be possible without their support. Lastly, I am deeply indebted to my wi fe Upama Dutta for tolerating my every mood during this whole process. She was besi de me in every step, in good things and most importantly when things were not good.
Table of Contents List of Tables. ii List of Figures iii Abstract.. v Chapter 1: Introduction. 1 Chapter 2: Materials and Methods. 6 Measurements. 8 Chapter 3: Results.. 11 Analysis of Prey-Size Stereotypy.. 11 Analysis of Prey Shell Thickness... 14 Analysis of Secondary Predation Pressure. 14 Analysis of Prey Chione Density 17 Chapter 4: Discussions. 18 Chapter 5: Conclusions. 25 Literatures Cited 27 i
List of Tables Table 1. Stratigraphic sequen ce of collection sites. indicates bulk samples 7 Table 2. Muricid prey-size stereotyp y, edge drilling fre quency (data taken from Dietl et al. 2004) and relative abundance of prey Chione across the studied stratigraphic form ations. Note that muricid prey-size stereotypy decreased simultaneously with increasing relative Chione abundance. Decline in muricid edge drilling behavior is not concurrent with change in prey-size stereotypy.................................................................................. 19 ii
List of Figures Figure 1. Measurements on the Chione valve. (A) prey valve height indicative of the prey size, (B) outer borehole diameter, indicative of the predator size. 9 Figure 2. Comparison of prey size selection between formations. Valve height is regressed on the outer bo rehole diameter. Color code follows: dark blue-Pinecrest member, Tamiami Fm. [lnH = 1.18 lnOBD +1.55 (R2= 0.63, p<0.001)] light blue-Caloosahat chee [lnH = 0.51 lnOBD + 2.56 (R2= 0.45, p<.0001)], redBermont [lnH = 0.73 lnOBD + 2.27 (R2= 0.49, p<.0001)], PinkFt. Thompson [lnH = 0.55 lnOBD + 2.49 (R2= 0.32, p<.0001)]. Note that the Tamiami Fm. is different than other formations in both slope and intercept. The slope a nd intercept did not vary from the Caloosahatchee Fm. to the Ft. Thompson Fm. R2 values, however, decreased at the end of Tamiami Fm and again at the end of the Ft. Thompson Fm 12 Figure 3. Comparison of muricid prey -size stereotypy between localities of each formation. (A) Pinecr est member, Tamiami Fm., (B) Caloosahatchee Fm., (C) Bermont Fm., (D) Ft. Thompson Fm. Note that outer borehole diameterprey valve height relation is least correlated in Ft. Thompson Formation. 13 Figure 4. Comparison of correlation-co efficient of prey-size stereotypy between localities of each formation. R2 values did not change significantly within samples of individual formations. However, there is a stepwise decrease in R2 value between-formations. 13 Figure 5. Valve thickness (lnTh) regressed on valve height (lnH). Color code follows: dark blue-Pinecrest member, Tamiami Fm. [lnTh = 0.94 lnH 2.63 (p<.0001)], light blue-Cal oosahatchee [lnTh = 0.87 lnH 2.44 (p<.0001)], redBermont [lnTh = 0.97 lnH 2.55 (p<.0001)], PinkFt. Thompson [lnTh = 1.24 lnH 3.38 (p<.0001)]. Note that the specimens from the Bermont Fm. are thicker th an the Pliocene formations. Ft. Thompson Fm. is different than others, indicating an increase in valve thickness from the middle Pleistocene... 15 iii
Figure 6. Comparison of edge-drilling fre quency and prey-s ize stereotypy. Color code follows: redmuricid edge drilling frequency; blue-muricid prey-size stereotypy. Note that edge-dri lling decreased sign ificantly across the Caloosahatchee-Bermont Fm. w ithout any change in prey-size stereotypy... 15 Figure 7. Comparison of prey Chione relative density and muricid preysize stereotypy. Color code follows: red Chione prey relative abundance; blue-muricid prey-size stereotypy (R2). Note that prey relative abundance increased from the Tamiami (0.7%) to the Caloosahatchee Fm. (55.84%) and at the Bermont Fm. (52.24%) Ft. Thompson Fm. (81.01%) 16 iv
Prey-size selectivity in the bivalve Chione in the Florida Pliocene-Pleistocene: A reevaluation Shubhabrata Paul ABSTRACT Previous study of drillin g predation on the bivalve Chione during the late Neogene of Florida suggested that prey-siz e selectivity of predators was disrupted by species turnover and morphological change within the prey genus. More recent experimental work, however, showed that at le ast some of these cha nges can be attributed to the confounding effects of facies sh ifts between naticid-dominated, muriciddominated, and mixed predator assemblages. As muricids have the most abundant and continuous fossil record and are most responsible for predation on the Chione bivalve in modern benthic ecosystems of Florida, we use new criteria to isolate the muricid component of the Chione drillhole record and analyze the hi story of this type of predator independently. Our analysis, based on drilled Chione from four Plio-Pleistocene formations in Florida, does not support the pr evious scenario of disruption at the end of the Pliocene followed by predator recovery. Rather, selected prey size has steadily increased since the middle Pliocene, alt hough the stereotypy of prey-size selection behaviors has decreased. In orde r to explain this trend, I perf ormed a series of statistical analyses to explore factors most likely to ha ve influenced muricid prey-size stereotypy. The timing of Species turnover within the pr ey lineage or change in prey phenotype does v
vi not correlate with the timing of changes in prey-size stereotypy and, therefore, cannot explain the observed changes in muricid behavior. Presence of secondary predators may also influence predator-prey interactions, because predators forage sub-optimally to ensure greater safety in th e presence of enemies. Resu lts indicate that secondary predation pressure decreased at the Ca loosahatchee-Bermont boundary without any evident change in muricid pr ey-size stereotypy and hence refute the hypothesis that secondary predation induced sub-optimal foragi ng. A third factor tested is prey density, which plays a major role in predator-prey in teractions in other systems by thwarting a predators ability to single out th e preferred individual prey. Increased Chione prey density correlates with and provides support for increased confusion among the muricid predators and hence driving the increased suboptimal behavior reflected by the increased variability in prey-size selection. This is the first time prey density effect has been considered and its importance here over all ot her factors suggests that it may be a critical factor in shortand long-term predator behavior trends in fossil record.
Chapter 1 Introduction The Late Neogene molluscan community of Florida experienced a regional extinction at the end of Plio cene, but the magnitudes of bi odiversity loss and ecological disruption as well as subsequent recove ry remain controversial (Woodring, 1966; Stanley, 1986; Vermeij and Petuch, 1986; Jackson et al., 1993; Petuch, 1995; Allmon et al., 1993, 1996; Roopnarine, 1996, 1997; A llmon, 2001; Doming, 2001; Todd et al., 2002). Dietl et al. (2004) suggest ed that the late Neogene ex tinction altered predator-prey interactions in the post-extinction molluscan community and that there was no evident recovery in last 2 myr. On the other hand, Roopnarine & Beussi nk (1999) suggested a recovery in the foraging behavior of pred atory gastropods from middle Pleistocene to recent. Here, I present a new da taset involving the prey bivalve Chione and borehole traces from muricid predators to determine th e magnitude of disruption in this predatorprey interaction across the extinction boundary and into the Pleistocene recovery interval. To assess the influence of the Late Ne ogene extinctions on this predator-prey interaction, Roopnarine and Beu ssink (1999) examined predat ory drillholes records from Chione valves in Plio-Pleistocene sediments of Fl orida. Drillholes on the bivalve shells are the most reliable indicators of ga stropod predation (Kelly and Hansen, 2003). Information regarding both prey size and pr edator size can be obt ained from a single 1
drilled valve. Previous studies (Kitchell et al., 1981) suggest that predatory gastropods are selective in choosing the prey size in order to maximize the net energy gain from drilling. Variability within the selected prey size is defined as the prey-size stereotypy. Roopnarine and Beussink (1999) suggested that predatory gastropods were more selective in preferred prey size in the pre-extinction Plio cene community, and prey-size stereotypy declined significantly in th e post-extinction Bermont community. They concluded that introduction of a new species due to a turnover within Chione occurred during an extinction event at the boundary between the Caloosahatchee and Bermont formations as the possible cause of the decline in prey stereotypy. However, Roopnarine and Beussink (1999) assumed that all drillholes were produced by naticid gastropods and overlooked the fact that some drillholes may have been produced by muricids. Daley et al. ( 2007) has shown that separating naticid and muricid drillhole traces results in different relationships reconstructed for predator-prey size selectivity. Failure to prope rly identify different predator s based on their traces risks confounding real trends in stereo typy with changes in the relative proportions of either predator type between time intervals. For example, Herbert and Dietl (2002, in prep.) suggest that drillholes on the umbonal region of Chione are produced by naticids exclusively. Muricid gastropods almost always drill at the central or ventral region of prey valves. Therefore, mixing predator iden tities may confound the prey-size stereotypy trend of predatory gastropods. Because muricids have the most conti nuous and abundant record of predatory interactions with the venerid bivalve Chione in the Neogene of Florida (Dietl et al. 2004), 2
we isolate the muricid-predator component of the Chione drillhole record on the basis of drillhole position following the approach of Herbert and Dietl (2002, in prep.). Because of its abundance, this in teraction is easier to quantify than the naticid-Chione and it is also presumably the more important from an evolutionary standpoint. Here, we present a new dataset involving Chione prey species and their muricid predator to determine the magnitude of disruption in this predator-p rey interaction across the ex tinction boundary and following recovery of biotic interaction. After reconstructing th e muricid-Chione interaction, we ask the question what are the factors that could cause the disruption in this predator-pre y relation. Other than turnover in prey or predator lineages, several eco logical factors can govern predator-prey interactions in general. Firstly, we discuss our results in the light of change in prey Chione shell thickness (Roopnarine and Beussin k, 1999). Prey shell thickness could be treated as a cost of dri lling by predatory gastropods (Kitchell et al ., 1981), where increasing thickness should drive selection of smaller, thinner prey or should interrupt stereotypy. Secondly, the presence of secondary predat ors could be treated as a potential factor in influencing the pred ator-prey interactions for predators in general (Brown and Kotler, 2004; Lima and Dill, 1990) and pred atory muricid gastropods in particular (Paul et al., in prep). Because predators generally prefer specific-sized prey to maximize energy gain ( Kitchell et al., 1981; Kowalewski, 2004) and likelihood of succe ss, introduction of a secondary predator should result in subop timal foraging, which may be expressed as increased variability in prey-s ize selection. In the present st udy, we test the applicability 3
of this hypothesis of secondary predation pressure as a driving factor of changes in our muricid-Chione interaction. Although this hypo thesis is valid in other predator-prey systems, it has not been tested in molluscan communities previously or considered in paleoecological studies of drilling predation. Lastly, we test the hypothesis that increasing prey density can play a pivotal role in modification of predator-prey interactions in ecological communities. Prey density has manifold influences in predator-prey inter actions, including the early warning of an approaching predator and in creased potential for escape (Treisman 1975; Treherne and Foster 1981), reduced probability of detec ting prey (Treisman 1975; Inman and Kerbs 1987), and increased confusion predators (Jeschke and To llrian 2007). According to Krause and Ruxton (2002) this c onfusion effect hinders a pred ators ability to single out individual optimal-size prey in dividuals. This hypothesis has also not been tested for molluscan communities; however, a number of other predator-prey systems support this argument (see Jeschke and Tollr ian 2007). Increases in prey density are known to reduce prey selectivity in the case of predators that locate prey us ing tactile or chemical sensing organs. The muricid gastropods studied here are chemosensory predators (Kitchell 1981). If prey density affects change in muricid pr ey-size stereotypy, we should expect to see sub-optimal foraging behavior or a decline in muricid prey-siz e stereotypy in the case of higher Chione relative abundance and th e opposite in times when Chione are less abundant. To test these three hypotheses, prey th ickness, presence of secondary predator s and prey density, I carried out a series of comparisons between changes in muricid prey4
size stereotypy with simultaneou s change in the po ssible governing factors. In an attempt to discern the processes underlying the change s in muricid prey-size stereotypy, we focus on the applicability and implications of these factors in the present study. 5
Chapter 2 Materials and Methods The age and stratigraphic relationships am ong different Pliocene-Pleistocene in Florida is still poorly unde rstood and in part controversial (Lyons 1991). Several researchers have proposed di fferent relationships between Tamami Formation and Pinecrest beds of Pliocene deposit (M ansfield, 1939; Olsson, 1964; Hunter, 1968; Brooks, 1974; DuBar, 1974; Petuch, 1982; Vokes, 1988). In the present study, I will follow Lyonss (1991) approach and use the name Tamiami Formation to refer to middle Pliocene deposits in Florida, and Pin ecrest beds is the uppermost member of the Tamiami Formation. The late Pliocene Caloos ahatchee Formation is distinguished from the Early Pleistocene Bermont Formation by th e extinction of Caloosahatchee index taxa at the Pliocene-Pleistocene boundary (Lyons 1991). The age of the Caloosahatchee Formation is tentatively placed between 2.5-1.8 myr (Bender, 1972, 1973). The age of the Bermont Formation is also controversial. Th e Bermont Formation ha s been placed in the Early Pleistocene (Vokes, 1963; Taylor, 1966; Walker, 1969; Hoerle, 1970) and also in the Middle Pleist ocene (DuBar, 1974 ; Blackwelder, 1981). The most recent evidence confirms the Early Pleistocene age (1.8-1.1 my r) of the Bermont Formation (Hulbert and Morgan, 1988; Webb et al., 1989). Ft. Thomps on Formation is assigned as the middle Pleistocene (Lyons 1991). Webb et al. (1989) suggested the age of 0.95-0.55 myr for the 6
Ft. Thompson Formation based on the Sr87/Sr86 isotope data. Howeve r, at least one study (Tiling, 2004) has assigned the age of 0.125 myr which is also the age of the last interglacial episode for the Ft. Thomps on formation from Caloosa Shell Pit. This stratigraphic framework was also followe d in other faunal studie s of Florida fossils (Roopnarine and Beussink 1999; Vermeij, 2005) with some difference, specifically by subdividing the Pinecrest beds into Upper and Lower Pinecrest beds (Petuch 1986, 2004). In the present study, I used samples collected from Pinecrest member, Tamiami Fm., the Caloosahatchee Fm., the Bermont Fm. and the Ft. Thompson Fm. Three sites were analyzed from each formation. Table 1 presents a synthesis of stratigraphic ranges of the collection sites with number of sa mples collected from each location. Table 1: Stratigraphic sequen ce of collection sites. indicates bulk samples. Stratigraphic Formation Stratigraphic range Location Sample no. Pinecrest member, Tamiami Fm. Middle Pliocene APAC Pit 32 Pinecrest member, Tamiami Fm. Middle Pliocene Mac Asphalt Pit 94 Pinecrest member, Tamiami Fm. Middle Pliocene Quality Aggregates Pit 118 Caloosahatchee Formation Late Pliocene Brantley Shell Pit 64 Caloosahatchee Formation Late Pliocene Bonita Grande Pit 199 Caloosahatchee Formation Late Pliocene Florida Shell & Dirt Pit 34 Bermont Formation Early Pleistocene Longan Lake 100 Bermont Formation Early Pleistocene GKK Pit 70 Bermont Formation Early Pleist ocene Florida Shell & Dirt Pit 92 Ft. Thompson Formation Middle Pleistocene Leisey Pit 120 Ft. Thompson Formation Middle Pleistocene Caloosa Shell Pit 60 Ft. Thompson Formation Middle Pleistocene Bermont Pit 57 7
Measurements: Three drilling parameters are measured on each Chione valve (Fig. 2). Prey size is measured as valve height. Studies have shown that outer borehole diameter can be used as a proxy of predator size in case of naticids (Kitchell et al., 1981) and muricid (Kowalewski, 2004) predatory gastropods. In th is study, predator size is assessed from the outer borehole diameter (OBD). Both prey valve height and outer drillhole diameter are measured with a slide calipers to the nearest 0.1 mm. Thickness of the prey Chione valve is measured with a screw gauge micrometer to nearest 0.1 mm. Data are transformed using natural log. When shell height is regressed relative to the OBD, the change in the y-intercept indicates a change in preferen ce for overall smaller or larger prey. A change in the slope indicates relative change in the range of selected prey sizes for juvenile and adult muricid predators. A low slope, for example, shows that juveniles and adult predators selected similarly-sized prey or lower prey-size selectivity. In other words, increasing selectivity (meaning increasingly selective foraging where juveniles and adults feed on very different size prey) is indicated by a steeper slope and lower y-intercept. Prey-size stereotypy refers to variability in selection and is determined as the correlation (R2) between predator and prey sizes for each formation. Ontogenetic change in thickness is measured by regressing shell thickness relative to shell height. When compared between formations, changes in th e slope of the regre ssion lines indicate relative change in thickness. Relationships between valve height, OBD and thickness 8
Figure 1: Measurements on the Chione valve. (A) prey valve height indicative of the prey size, (B) outer borehole diameter, indicative of the predator size. were determined using Model I regression. Mu ricid prey-size stereo typy was measured in two different ways(1) different sites with in a formation considered in unison (i.e. pooled), (2) considering differe nt sites within a formati on individually (i.e. non-pooled) Predatory muricid gastropods use edge-dri lling in the presence of secondary predators (Paul et al., in prep) and competito rs (Dietl et al., 2004; Dietl and Herbert, 2005). We used the frequency of muricid edge-drilling on Chione as a proxy for secondary predation pressure. This dataset was taken from Dietl et al. (2004). Edgedrilling frequency is measured as: (number of edge drilled valve/number of total drilled valves)*100. Chione relative density is determined from its abundance rela tive to all prey 9
10 ts uates (REU) 2004-2007 programs run at USF and by the author in 2008. bivalves in the various bulk samples studied. Bulk samples were collected by participan in the NSF-funded Research Experience for Undergrad
11 Chapter 3 Results nalysis of Prey-Size Stereotypy ses ne Ft. ilarly er muricids so that both small and large pr A When prey size (valve height) is regressed relative to predator size (as inferred by OBD) for each formation (Fig. 2), the slope of the least square re gression line decrea significantly (t-value 10.56, p<0.001) after the middle Pliocene Tamiami Formation indicating a decrease in prey-s ize selectivity (difference between selected prey size for juvenile and adult predator). The slope of th e regression line increases minimally (t-value -3.92, p<0.001) from across the Caloosahatchee-Bermont boundary. There is no evident change in the slope between the early Pleist ocene Bermont and the middle Pleistoce Thompson formation (t-value 2.40, p>0.001). Although the slope de clines after the Tamiami formation, intercept of the regres sion line increase from the Tamiami to Caloosahatchee formation. Thus, different sizes of muricid predators preyed on sim sized Chione following the middle Pliocene, with the bulk of this shift reflecting a general increase in the size of prey selected by small edators fed on a similar size range of prey. Model I regression analysis of prey si ze on drillhole size for pooled samples indicates that prey-size ster eotypy was reduced (i.e., vari ability of selection also
12 measured een the Early Pleistocene Bermont Fm. and the middle Pleistocene Ft. Thompson Fm. e and intercept. The slope and intercept did not vary from the Caloosahatchee Fm. to the Ft. Thompson Fm. R2 values, however, decreased at the end of Tamiami Fm. and again at the end of the Ft. Thompson Fm. increased) in two steps. The correlation betw een prey-size and predator size as by R2, decreased at the Tamiami-Caloosahatchee boundary from 0.63 to 0.45. Interestingly, prey stereot ypy did not change substantiall y across the main extinction boundary between the Latest Pliocene Caloosahatchee Fm. and the Bermont Fm. as R 2 values for these units are nearly identical (0.45 to 0.49). Another decrease in prey-size stereotypy from 0.49 to 0.32 took place betw Fig. 2 Comparison of prey size selection between formations. Valve height is regressed on the outer borehole diameter. Color code follows: dark blue-Pinecrest member, Tamiami Fm. [lnH = 1.18 lnOBD +1.55 (R2= 0.63, p<0.001)] light blue-Caloosahatchee [lnH = 0.51 lnOBD + 2.56 (R2= 0.45, p<.0001)], redBermont [lnH = 0.73 lnOBD + 2.27 (R2= 0.49, p<.0001)], PinkFt. Thompson [lnH = 0.55 lnOBD + 2.49 (R2= 0.32, p<.0001)]. Note that the Tamiami Fm. is different than other formations in both slop 2 2.2 2.4 2.6 2.8 3 3.2 3.4 0.50.60.70.80.922.214.171.124.4 ln outer borehole diameterln valve height
13 2 2.2 2.4 2.6 2.8 3 3.2 3.4 3.6 0.40.60.81126.96.36.199 Brantley Shell Pit Florida Shell & Dirt Pit Bonita Grande Pit 2 2.2 2.4 2.6 2.8 3 3.2 3.4 3.6 0.40.60.81188.8.131.52 Caloosa Shel Pitl Leisley Pit Bermont Pit 2 2.2 2.4 2.6 2.8 3 3.2 3.4 3.6 0.40.60.81184.108.40.206 GKK Pit Florida Shell & Dirt Pit Longan Lake Pit 2 2.2 2.4 2.6 2.8 3 3.2 3.4 3.6 0.40.60.81220.127.116.11 Mac Asphalt Pit Quality Aggregates APAC Pit A B C D Fig. 3: Comparison of muricid prey-size stereotypy between localities of each formation. (A) Pinecrest member, Tamiami Fm., (B) Caloosahatchee Fm., (C) Be rmont Fm., (D) Ft. Thompson Fm. Note that outer borehole diameterprey valve height relation is least correlated in Ft. Thompson Formation. 0 0. 1 0. 2 0. 3 0. 4 0. 5 0. 6 0. 7 0. 8 0. 9Ma c As p h al t QA P i t AP AC Pi t P o ol ed B r an t l ey S h e l l F SD un i t 1 B oni t a G r ande P o ol ed Gk k P i t F SD un i t 3 Lo n ga n la k e P o ol ed C al oo sa S h e l l Le i s l e y P it Be r m o n t P i t P o ol ed Caloosahatchee Berm ont Ft. T hom p son Pinecres t Fig. 4: Com p arison of c o rrelation-co e fficient of prey-size se lection be t w ee n localities of each form at ion. R2 val u es di d not chan ge si gni fi cant l y wi t h i n s a m p l e s of i n di vi d u al f o rm at ions H o weve r, t h ere i s a st ep wi se decrease in R2 val u e b et wee n -f orm a t i ons.
When samples from different localities (within a formation) are pooled, a locality with a larger sample size ma y have more influence on the mean value for the formation than a locality with smaller sample size. To examine the extent of variability between different localities of the same formation, we performed prey-size selection analysis on different localities individually (Fig. 3). Our results show th at within each individual formation, prey-size stereotypy (R2) did not vary between differe nt localities (Fig. 4). It indicates that our pooled result s (Fig. 2) are not influenced by any single locality result. Analysis of Prey Shell Thickness When shell thickness is regressed against shell height (Fig. 5), the Tamiami Fm. and the Caloosahatchee Fm. do not differ in shell thickness. The slope and intercept remained nearly identical in these formations Prey shell thickness increased in the Early Pleistocene Bermont Fm. Although intercept did not change significantly, the slope of the regression line increased from the preceding Pliocene formations. Major increase in the prey shell thickness occurred by the middle Pleistocene Ft. Thompson Fm. The slope and intercept of the regression line are differen t from those of preceding formations. Analysis of Secondary Predation Pressure Results (Table 2, Fig. 6) show th at edge-drilling fr equency declined significantly at the PliocenePleistocene boundary from 4.37% to 0% (Chi-square test, 14
15 -1 -0.8 -0.6 -0.4 -0.2 0 0.2 0.4 0.6 0.8 1 18.104.22.168.93.13.3 ln valve heightln thickness Fig. 5: Valve thickness (lnTh) regressed on valve hei ght (lnH). Color code follows: dark blue-Pinecrest member, Tamiami Fm. [lnTh = 0.94 lnH 2.63 (p<.0001)], light blue-Caloosahatchee [lnTh = 0.87 lnH 2.44 (p<.0001)], redBermont [lnTh = 0.97 lnH 2.55 (p<.0001)], PinkFt. Thompson [lnTh = 1.24 lnH 3.38 (p<.0001)]. Note that the specimens from the Bermont Fm. are thicker than the Pliocene formations. Ft. Thompson Fm. is different than others, indicating an increase in valve thickness from the middle Pleistocene. 0 2 4 6 8 10 0 0.2 0.4 0.6 0.8 1PinecrestCaloosahatcheeBermontFt. ThompsonEdge drilling frequencyPrey-size stereotypy Fig. 6: Comparison of edge-drilling frequency and pr ey-size stereotypy. Color code follows: rededge drilling frequency; blue-prey-size stereotypy. Note that edge-drilling decreased significantly across the Caloosahatchee-Bermont Fm. without any change in prey-size stereotypy.
p<0.05). Edgedrilling frequency also declin ed from 9.69% in the middle Pliocene Tamiami to 4.37% in the Caloosahatchee, bu t this difference was not statistically significant (Chi-square test, p>0.05). The absence of any edge-drilled Chione in the Pleistocene indicates a decline in seconda ry predation or competition pressure on predatory muricid gastropods. In comparison wi th the results of our prey-size stereotypy analysis, muricids were most stereotyped with respect to prey-size in the middle Pliocene Tamiami Fm., when secondary predation pressu re was also highest. Muricid prey-size stereotypy also declined at th e end of the Tamiami Fm. and also at the end of the Ft. Thompson Fm. but without any evident cha nge in secondary predation pressure. 0 20 40 60 80 100 0 0.2 0.4 0.6 0.8 1PinecrestCaloosahatcheeBermontFt. ThompsonRelative prey Chione densityMuricid prey-size stereotypy Fig. 7: Comparison of prey Chione relative density and prey-size stereotypy. Color code follows: red Chione prey relative abundance; blue-prey-size stereotypy (R2). Note that prey relative abundance increased from the Tamiami (0.7%) to the Caloosahatchee Fm. (55.84%) and at the Bermont Fm. (52.24%) Ft. Thompson Fm. (81.01%). 16
Analysis of Prey Chione Density Our results (Table 2, Fig. 7) show that the relative Chione abundance (total number of Chione/total number of prey bivalves) increased significantly (Chi-square test, p< 0.05) between the middle Pliocene Tamiami Formation (<1% of all bivalves) and the Late Pliocene Caloosahatchee Formation (5 5% of all bivalves). Although Pliocene C. erosa was replaced by Pleistocene C. elevata in the Bermont formation, there was no significant change in relative Chione density at this time (Chi-square test, p<0.05) (52% of all bivalves in Bermont formation). Anothe r significant increase in prey density took place between the Early Pleistocene Berm ont Fm. and the middle Pleistocene Ft. Thompson Fm (Chi-square test, p< 0.05) (81% of all bivalves). 17
Chapter 4 Discussions Regression analyses do not support the results of Roopnarine and Beussink (1999). They suggested that predator-prey intera ctions were disrupted by prey turnover at the Caloosahatchee-Bermont boundary and r ecovered by the middle Pleistocene. By contrast, we observe an earlier shift in muricid prey-size selectivity as well as an earlier and a later decline in prey -size stereotypy. These change s cannot be explained by the replacement of Pliocene C. erosa by the Pleistocene C. elevata which occurred at the end of the Caloosahatchee Formation ( Roopnarine, 1995, 2001; Vermeij and Roopnarine, 2000). Although C. erosa was replaced by the C. elevata in post-Pliocene Florida molluscan community, C. elevata was not more escalated than the pre-extinction C. erosa (Roopnarine and Beussink, 1999). Our results su ggest that any morphological differences between C. erosa and its replacement C. elevata did not pose novel challenges for muricid predators and did not interrupt their prey-foraging or prey-handling behaviors. Other than species turnover within a prey or predator lineage, a number of factors can potentially influence interactions in a specifi c system. In order to evaluate the role of these factors, I performed independent analyses of these factors and then compared the results with change in muricid-prey st ereotypy results. Results suggest that Chione shell thickness increased with simultaneous decline in murici d prey-size stereotypy at the 18
Table 2: Muricid prey-size stereotypy, edge drilling frequency (data taken from Dietl et al. 2004) and relative abundance of prey Chione across the studied stratigraphic form ations. Note that muricid prey-size stereotypy decreased simultane ously with increasing relative Chione abundance. Decline in muricid edge drilling behavior is not concurrent w ith change in prey-size stereotypy. Stratigraphic Formation Muricid preysize stereotypy Edge drilling frequency Relative Chione density Pinecrest member, Tamiami Fm. 0.63 9.69 0.70 Caloosahatchee Formation 0.45 4.37 55.84 Bermont Formation 0.49 0 52.24 Ft. Thompson Formation 0.32 0 81.01 Bermont-Ft. Thompson boundary. Therefore, an in crease in thickness ca nnot be ruled out as a potential factor driving the decline in prey-size stereotypy at the end of the Bermont Fm. However, a causal relationship between these two factors can be rejected by two lines of argument. First, a change in the prey size-thickne ss relation after the Caloosahatchee was accompanied by no changes in predator behavior. Secondly, changes in predator behavior after the Tamiami were not accompanied by changes in prey thickness. Therefore, the co rrelation between thickness and pr edator behavior after the Bermont appears to be coincidental only. Increasing variability for prey-size sele ction can be viewed as increasing suboptimal foraging for a specific predator In the presence of enemies, foragers typically decrease risk through reduced activity, shif ting to less productive but safer habitats, restricting foraging time to reduc e exposure time, or foraging in similar habitats but with less selectivity (H ouston et al., 1993; Walters and Juanes, 1993; Brown, 1999; Kotler et al., 2004; Heithaus et al., 2007 ) For example, foragers reduce their foraging activity in order to gain greater safety in pr esence of enemies. Mule deer ( Odocoileus hemionus) 19
spent less time in foraging in high rick areas. This risk factor comes from the secondary predation pressure of mountain lions ( Puma Concolor) ( Altendorf et al., 2001 ). A shifting of habitat is found with in green sea turtle ( Chelonia mydas ) community as a response of the predation pressure from tiger sharks ( Galeocerdo cuvier ). Green sea turtles forage in low quality seagrass when tier shark is abunda nt. When number of tig er shark is reduced, i.e., in time of less predation pressure turtles are found to forage in high quality seagrass near to the river banks (Heithaus et al., 2007) A forager may also restrict foraging time to reduce exposure time to enemies. Experime ntal study (Paul et al.,in prep) show that predatory snail Chicoreus dilectus attacks on the edge of their clam prey Chione elevata at least two-times higher in presence of sec ondary predators such as crabs. This edgedrilling technique shortens the foraging time and subsequently the exposure time to enemies. I tested the possibility that increasing predation pressu re on muricid gastropods is driving sub-optimal foraging, and hence decline in prey-size stereotypy. Higher edgedrilling frequency indicates higher secondary predation pressure in the Pliocene molluscan community. My preliminary predicti on was that any decr ease in secondary predation pressure should have been accompanied by an increase prey-size stereotypy. My results do not support this prediction. Muri cids were most stereotyped (prey-size) in the middle Pliocene Tamiami Fm., when our ed ge-drilling proxy for secondary predation pressure was also highest. This is opposite of the predic tion. Muricid prey-size stereotypy also declined at the Tamiami-Caloosahat chee as well as the Bermont-Ft. Thompson boundary without any evident change in sec ondary predation pressure. These results 20
refute the hypothesis that secondary predat ion induced sub-optimal foraging over last 3 Ma in this predator-prey system. Predator-prey interactions can also be influenced by changing prey-density. A predator becomes confused when faced with higher number of prey. For example, Jeschke and Tollrian study ( 2007) suggest that, larvae of Aeshna cyanea becomes less efficient predator when Daphnia magna prey density gradually increases from 10 to 250. This negative correlation between attack efficiency and prey density indicates the increasing confusion factor among the Aeshna cyanea larvae. Confusion factor also increases with higher prey density in case of Chaoborus obscuripes predator and Daphnia obtuse prey (prey density changed gradually from 5 to 70). In both of these two cases negative correlation between attack e fficiency and prey density indicates that predator forage less efficien tly (i.e., sub-optimally) with increasing prey density. Predator confusion is a widespread res ponse when faced with higher prey density (Jeschke and Tollrian 2007). Fa iling to single out individual prey results in sub-optimal foraging behavior of different ta ctile, visual and chemosensory predators. If this true for our system, we expect to see that predatory muricids became more confused, as reflected in decreased prey-size stereotypy, wh en faced with higher number of Chione Comparison of prey Chione density with prey-size stereotypy shows a pattern that supports this hypothesis. Muri cid prey-size stereotypy was highest in the Tamiami Fm. when relative Chione density was lowest. Muricids were least selective in choosing the prey size in the Ft. Thompson Fm. when Chione was most available. Moreover, stasis in prey-size stereotypy coin cided with stasis in Chione prey abundance between the 21
Caloosahatchee and Bermont Fm. In addition to these, comparison of prey Chione density with prey stereotypy shows that neither parameter was influenced by the species turnover event at the Caloos ahatchee-Bermont boundary. Th ese results indicate that increase in prey density cannot be ruled out as a potential factor in driving the changes in muricid prey-size stereotypy. This argument is supported by another lin e of evidence. Studies suggest that confusion factor decreases when the prey popul ation contains a grea ter variety of prey types, including presence of odd individuals (Ohguchi, 1981; Landeau and Terborgh, 1986; Krakauer, 1995; Tosh et al., 2006). For example, hyenas spend a cons iderable time in choosing their prey during hunting. Usually hyenas hunt old or weak individuals. When Kruuk placed a marker on some of the individuals within the prey group, hyenas almost always targeted those odd, marked in dividuals (Kruuk, 1972). This variety of prey types may also refer to the availability of prey of different genera (Jeschke and Tollrian, 2007). A predator faces more prey types when species abundances within the prey community are more even (i.e. each prey genus is represented be nearly similar number of individuals) and hence conf usion factor will be reduced. As Chione dominance relative to other bivalve prey incr eased after the Pinecrest, we would expect a decrease of prey community evenness and hence increasing confus ion factor within predatory muricid gastropods. Further work is needed to test this hypothesis in detail. Although this study is an important step in understanding the nature of predatory response in face of changing prey density in molluscan community, these results also raise the question about the magnitude of muricid predation intensity on Chione Kelly 22
and Hansen (1996) argued that decline in pr edator behavioral ster eotypy is associated with higher drilling frequenc y. This argument was based on the assumption of selective removal of highly escalated prey immediat ely after the mass th e mass extinction. In Neogene Florida, the Pliocene C. erosa was not more escalated than the Pleistocene C. elevata So, decline in predator behavioral stereotypy in the studied stratigraphic formations was not due to the change in ma gnitude of prey escalation. If we consider increased variability in prey -size stereotypy as the reflec tion of increased sub-optimal foraging behavior driven by in creased confusion factor for muricid gastropods, we would expect to see a decline in predation intensity on Chione relative to other available prey types. With suboptimal foraging, foraging ti me should go up and prey consumed per unit time should go down only when muricids are foraging on Chione not other bivalves. This factor may result in decline in predati on intensity on Chione re lative to other prey bivalves. However, present lineage-level dataset is insufficient to test this hypothesis. Assemblage-level dataset is required to conclusively answer this question. Beyond predation intensity, sub-optimal fo raging may be reflected through other parameters like frequency of unsuccessful att ack. As this study sugge sts that sub-optimal foraging behavior of predatory muricid gastropods may be driven by increased confusion to identify the preferred prey size class, we expect to see an increase in frequency of the unsuccessful attacks. In a review of the incomplete or multiple drillholes on bivalves, indicating prey effectiveness, Kelly and Ha nsen (2003) found that frequency of failed attacks increased from the Cretaceous to the Oligocene indicating that predatory gastropods became less effective in handling prey in the Oligocene. Following Vermeijs 23
escalation hypothesis (1987) th ey suggested that the incr ease in failed attacks was a reflection of the increasing effectiveness of prey anti-predatory traits (e.g. shell thickness) relative to predator efficiency. However, none of these studies examined relative prey density in relation to the failed attack or prey effectivene ss. The present study indicates that increasing prey density effect may play an important role in determining predator efficiency. Future work will be aimed to test the hypothesis. 24
Chapter 5 Conclusions Previous study of predation on Chione prey was confounded by the mixed signature of naticid and muri cid foraging behavior. As, muricids are the most common predators of the Chione bivalve in Neogene fossil reco rd and modern ecosystem in Florida, present study deals with the independe nt muricid component of the fossil record. Present study suggests that in the muricidChione system, prey-size stereotypy declined at the Tamiami-Caloosahatchee boundary as well as at the Bermont-Ft. Thompson boundary. There was no evident change in muricid prey-size stereotypy at the Caloosahatchee-Bermont boundary. These results indicate that a late Neogene regional extinction did not alter muri cid prey-size stereotypy. This trend cannot be explained by the prey species turnover event at the PliocenePleistocene boundary. Increased sub-optimal foraging behavior of muricids at the Tamiami-Caloosahatchee boundary cannot be ex plained by the change in prey phenotype (shell thickness). Muricid pr ey-size stereotypy declined at the end of the Tamiami Fm. without any evident change in prey thickness. At the Ca loosahatchee-Bermont boundary, thickness increased w ithout any increase in sub-optim al foraging behavior. Although, Chione shell thickness increased simultaneously with the decline in prey-size stereotypy at the BermontFt. Thompson boundary, the corr elation between thickness and predator 25
behavior after the Bermont appear s to be coincidental only. Increased variability of prey-size sel ection after the middle Pliocene was not a reflection of change in secondary predation pressure on the muricid gastropods. Muricids expressed optimal foraging behavior when secondary predation pressure was highest in the Tamiami formation. Secondary predation pr essure decreased significantly at the end of Caloosahatchee formation wit hout any evident change in muricid prey-s ize stereotypy. Increased prey density may cause the in creased confusion f actor within the predators to select the preferred prey-size cl ass and hence driving th e decline of prey-size stereotypy. Relative abundance of Chione prey increased simultaneously with decrease in muricid prey-size stereotypy. My results suggest that temporal patt ern of prey density plays a more important role than species-replacement within the prey lineage or change in prey phenotype or influence of secondary predation pressure in our specific muricid predator-Chione prey system. 26
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